Louise A. Rollins-Smith, Ph.D.

Professor

louise.rollins-smith@vanderbilt.edu
Faculty Appointments
Professor of Pathology, Microbiology and Immunology Professor of Biological SciencesProfessor of Pediatrics
Education
Ph.D., Zoology, University of Minnesota, Minneapolis, MinnesotaM.S., Zoology, University of Minnesota, Minneapolis, MinnesotaB.A., Biology, Hamline University, Saint Paul, Minnesota
Office Address
A5102-A Medical Center North
Nashville, TN 37232
Research Description
The main focus of my research is host and pathogen interactions using amphibian model systems. Our work also falls into the category of Eco-Immunology. Currently, my laboratory is pursuing a number of questions concerning the nature of innate and adaptive immune defenses in frog skin against two novel chytrid pathogens linked to global amphibian declines. Understanding the immune defense mechanisms of amphibians has taken on increased importance in recent years because of the urgent problem of global amphibian declines. Little is known about the conventional adaptive immune response against Batrachochytrium dendrobatidis (Bd) and a recently discovered closely related chytrid, Batrachochytrium salamandrivorans (Bsal). Our ongoing studies have shown that Bd releases factors which inhibit immune cells including lymphocytes and macrophages. Additional studies showed that Bsal also releases factors that inhibit immunity. Current research investigates the specific mechanisms by which these fungi may escape immune clearance. Another focus of my research is the study of antimicrobial peptides in frog skin in defense against bacterial, viral, and fungal pathogens. Currently, we are using growth inhibition assays to test the ability of purified antimicrobial peptides and mixtures of skin peptides to interfere with growth of specific pathogens that have been associated with global amphibian declines. Another area of research is the effects of temperature on immune defenses of local Tennessee amphibians. This relates to the question of how climate change may impact southern amphibians. With collaborators, we are also studying the role of skin microbiota as protectors of amphibians from Bd and Bsal.


Research Keywords
Innate Immune Defenses. Host and pathogen interactions. Immune defenses against Batrachochytrium dendrobatidis. Immune defenses against Batrachochytrium salamandrivorans. Global amphibian declines. Skin microbiota. Antimicrobial peptides. Climate change research.
Publications
Pokidysheva EN, Redhair N, Ailsworth O, Page-McCaw P, Rollins-Smith L, Jamwal VS, Ohta Y, Bächinger HP, Murawala P, Flajnik M, Fogo AB, Abrahamson D, Hudson JK, Boudko SP, Hudson BG. Collagen IV of basement membranes: II. Emergence of collagen IVa345 enabled the assembly of a compact GBM as an ultrafilter in mammalian kidneys. J Biol Chem [print-electronic]. 2023 Dec; 299(12): 105459. PMID: 37977222, PMCID: PMC10746531, PII: S0021-9258(23)02487-0, DOI: 10.1016/j.jbc.2023.105459, ISSN: 1083-351X.

Rollins-Smith LA, Le Sage EH. Heat stress and amphibian immunity in a time of climate change. Philos Trans R Soc Lond B Biol Sci [print-electronic]. 2023 Jul 7/31/2023; 378(1882): 20220132. PMID: 37305907, PMCID: PMC10258666, DOI: 10.1098/rstb.2022.0132, ISSN: 1471-2970.

Rollins-Smith LA. The importance of antimicrobial peptides (AMPs) in amphibian skin defense. Dev Comp Immunol [print-electronic]. 2023 May; 142: 104657. PMID: 36754220, PII: S0145-305X(23)00027-7, DOI: 10.1016/j.dci.2023.104657, ISSN: 1879-0089.

Katzenback BA, Rollins-Smith LA. Uncovering the fascinating world of amphibian immunity [editorial]. Dev Comp Immunol [print-electronic]. 2023 May; 142: 104655. PMID: 36739929, PII: S0145-305X(23)00025-3, DOI: 10.1016/j.dci.2023.104655, ISSN: 1879-0089.

Hardman RH, Reinert LK, Irwin KJ, Oziminski K, Rollins-Smith L, Miller DL. Disease state associated with chronic toe lesions in hellbenders may alter anti-chytrid skin defenses. Sci Rep. 2023 Feb 2/3/2023; 13(1): 1982. PMID: 36737574, PMCID: PMC9898527, PII: 10.1038/s41598-023-28334-4, DOI: 10.1038/s41598-023-28334-4, ISSN: 2045-2322.

Wilber MQ, Ohmer MEB, Altman KA, Brannelly LA, LaBumbard BC, Le Sage EH, McDonnell NB, Muñiz Torres AY, Nordheim CL, Pfab F, Richards-Zawacki CL, Rollins-Smith LA, Saenz V, Voyles J, Wetzel DP, Woodhams DC, Briggs CJ. Once a reservoir, always a reservoir? Seasonality affects the pathogen maintenance potential of amphibian hosts. Ecology [print-electronic]. 2022 Sep; 103(9): e3759. PMID: 35593515, DOI: 10.1002/ecy.3759, ISSN: 1939-9170.

Rollins-Smith LA, Reinert LK, Le Sage M, Linney KN, Gillard BM, Umile TP, Minbiole KPC. Lymphocyte Inhibition by the Salamander-Killing Chytrid Fungus, Batrachochytrium salamandrivorans. Infect Immun [print-electronic]. 2022 Mar 3/17/2022; 90(3): e0002022. PMID: 35130454, PMCID: PMC8929357, DOI: 10.1128/iai.00020-22, ISSN: 1098-5522.

Rollins-Smith LA, Le Sage EH. Batrachochytrium fungi: stealth invaders in amphibian skin. Curr Opin Microbiol [print-electronic]. 2021 Jun; 61: 124-32. PMID: 33964650, PII: S1369-5274(21)00047-3, DOI: 10.1016/j.mib.2021.04.002, ISSN: 1879-0364.

Carter ED, Bletz MC, Le Sage M, LaBumbard B, Rollins-Smith LA, Woodhams DC, Miller DL, Gray MJ. Winter is coming-Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans. PLoS Pathog. 2021 Feb; 17(2): e1009234. PMID: 33600433, PMCID: PMC7891748, PII: PPATHOGENS-D-20-02036, DOI: 10.1371/journal.ppat.1009234, ISSN: 1553-7374.

Le Sage EH, LaBumbard BC, Reinert LK, Miller BT, Richards-Zawacki CL, Woodhams DC, Rollins-Smith LA. Preparatory immunity: Seasonality of mucosal skin defences and Batrachochytrium infections in Southern leopard frogs. J Anim Ecol [print-electronic]. 2021 Feb; 90(2): 542-54. PMID: 33179786, DOI: 10.1111/1365-2656.13386, ISSN: 1365-2656.

Rodriguez C, Ibáñez R, Rollins-Smith LA, Gutiérrez M, Durant-Archibold AA. Antimicrobial Secretions of Toads (Anura, Bufonidae): Bioactive Extracts and Isolated Compounds against Human Pathogens. Antibiotics (Basel). 2020 Nov 11/26/2020; 9(12): PMID: 33255881, PMCID: PMC7761505, PII: antibiotics9120843, DOI: 10.3390/antibiotics9120843, ISSN: 2079-6382.

Rollins-Smith LA, Smith PB, Ledeczi AM, Rowe JM, Reinert LK. Caerin 1 Antimicrobial Peptides That Inhibit HIV and Neisseria May Spare Protective Lactobacilli. Antibiotics (Basel). 2020 Sep 9/30/2020; 9(10): PMID: 33008028, PMCID: PMC7600266, PII: antibiotics9100661, DOI: 10.3390/antibiotics9100661, ISSN: 2079-6382.

Lambert MR, Womack MC, Byrne AQ, Hernández-Gómez O, Noss CF, Rothstein AP, Blackburn DC, Collins JP, Crump ML, Koo MS, Nanjappa P, Rollins-Smith L, Vredenburg VT, Rosenblum EB. Comment on "Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity". Science. 2020 Mar 3/20/2020; 367(6484): PMID: 32193293, PII: 367/6484/eaay1838, DOI: 10.1126/science.aay1838, ISSN: 1095-9203.

Woodhams DC, Rollins-Smith LA, Reinert LK, Lam BA, Harris RN, Briggs CJ, Vredenburg VT, Patel BT, Caprioli RM, Chaurand P, Hunziker P, Bigler L. Probiotics Modulate a Novel Amphibian Skin Defense Peptide That Is Antifungal and Facilitates Growth of Antifungal Bacteria. Microb Ecol [print-electronic]. 2020 Jan; 79(1): 192-202. PMID: 31093727, PII: 10.1007/s00248-019-01385-9, DOI: 10.1007/s00248-019-01385-9, ISSN: 1432-184X.

Robak MJ, Reinert LK, Rollins-Smith LA, Richards-Zawacki CL. Out in the cold and sick: low temperatures and fungal infections impair a frog's skin defenses. J Exp Biol. 2019 Sep 9/23/2019; 222(Pt 18): PMID: 31488625, PII: jeb.209445, DOI: 10.1242/jeb.209445, ISSN: 1477-9145.

Rollins-Smith LA, Ruzzini AC, Fites JS, Reinert LK, Hall EM, Joosse BA, Ravikumar VI, Huebner MI, Aka A, Kehs MH, Gillard BM, Doe E, Tasca JA, Umile TP, Clardy J, Minbiole KPC. Metabolites Involved in Immune Evasion by Batrachochytrium dendrobatidis Include the Polyamine Spermidine. Infect Immun [electronic-print]. 2019 Mar; 87(5): PMID: 30833338, PMCID: PMC6479046, PII: IAI.00035-19, DOI: 10.1128/IAI.00035-19, ISSN: 1098-5522.

Kueneman JG, Bletz MC, McKenzie VJ, Becker CG, Joseph MB, Abarca JG, Archer H, Arellano AL, Bataille A, Becker M, Belden LK, Crottini A, Geffers R, Haddad CFB, Harris RN, Holden WM, Hughey M, Jarek M, Kearns PJ, Kerby JL, Kielgast J, Kurabayashi A, Longo AV, Loudon A, Medina D, Nuñez JJ, Perl RGB, Pinto-Tomás A, Rabemananjara FCE, Rebollar EA, Rodríguez A, Rollins-Smith L, Stevenson R, Tebbe CC, Vargas Asensio G, Waldman B, Walke JB, Whitfield SM, Zamudio KR, Zúñiga Chaves I, Woodhams DC, Vences M. Community richness of amphibian skin bacteria correlates with bioclimate at the global scale. Nat Ecol Evol [print-electronic]. 2019 Mar; 3(3): 381-9. PMID: 30778181, PII: 10.1038/s41559-019-0798-1, DOI: 10.1038/s41559-019-0798-1, ISSN: 2397-334X.

Martin H C, Ibáñez R, Nothias LF, Boya P CA, Reinert LK, Rollins-Smith LA, Dorrestein PC, Gutiérrez M. Viscosin-like lipopeptides from frog skin bacteria inhibit Aspergillus fumigatus and Batrachochytrium dendrobatidis detected by imaging mass spectrometry and molecular networking. Sci Rep. 2019 Feb 2/28/2019; 9(1): 3019. PMID: 30816229, PMCID: PMC6395710, PII: 10.1038/s41598-019-39583-7, DOI: 10.1038/s41598-019-39583-7, ISSN: 2045-2322.

Flechas SV, Acosta-González A, Escobar LA, Kueneman JG, Sánchez-Quitian ZA, Parra-Giraldo CM, Rollins-Smith LA, Reinert LK, Vredenburg VT, Amézquita A, Woodhams DC. Microbiota and skin defense peptides may facilitate coexistence of two sympatric Andean frog species with a lethal pathogen. ISME J [print-electronic]. 2019 Feb; 13(2): 361-73. PMID: 30254321, PMCID: PMC6331565, PII: 10.1038/s41396-018-0284-9, DOI: 10.1038/s41396-018-0284-9, ISSN: 1751-7370.

Rollins-Smith LA, Robert J. Lymphocyte Deficiency Induced by Sublethal Irradiation in Xenopus. Cold Spring Harb Protoc. 2019 Jan 1/2/2019; 2019(1): PMID: 30104411, PII: pdb.prot097626, DOI: 10.1101/pdb.prot097626, ISSN: 1559-6095.

Tennessen JB, Parks SE, Swierk L, Reinert LK, Holden WM, Rollins-Smith LA, Walsh KA, Langkilde T. Frogs adapt to physiologically costly anthropogenic noise. Proc Biol Sci. 2018 Nov 11/21/2018; 285(1891): PMID: 30464067, PMCID: PMC6253376, PII: rspb.2018.2194, DOI: 10.1098/rspb.2018.2194, ISSN: 1471-2954.

Voyles J, Woodhams DC, Saenz V, Byrne AQ, Perez R, Rios-Sotelo G, Ryan MJ, Bletz MC, Sobell FA, McLetchie S, Reinert L, Rosenblum EB, Rollins-Smith LA, Ibáñez R, Ray JM, Griffith EJ, Ross H, Richards-Zawacki CL. Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation. Science. 2018 Mar 3/30/2018; 359(6383): 1517-9. PMID: 29599242, PII: 359/6383/1517, DOI: 10.1126/science.aao4806, ISSN: 1095-9203.

Rodríguez C, Rollins-Smith L, Ibáñez R, Durant-Archibold AA, Gutiérrez M. Toxins and pharmacologically active compounds from species of the family Bufonidae (Amphibia, Anura). J Ethnopharmacol [print-electronic]. 2017 Feb 2/23/2017; 198: 235-54. PMID: 28034659, PII: S0378-8741(16)32373-X, DOI: 10.1016/j.jep.2016.12.021, ISSN: 1872-7573.

Rollins-Smith LA. Amphibian immunity-stress, disease, and climate change. Dev. Comp. Immunol [print-electronic]. 2017 Jan; 66: 111-9. PMID: 27387153, PII: S0145-305X(16)30219-1, DOI: 10.1016/j.dci.2016.07.002, ISSN: 1879-0089.

Rebollar EA, Antwis RE, Becker MH, Belden LK, Bletz MC, Brucker RM, Harrison XA, Hughey MC, Kueneman JG, Loudon AH, McKenzie V, Medina D, Minbiole KP, Rollins-Smith LA, Walke JB, Weiss S, Woodhams DC, Harris RN. Using "Omics" and Integrated Multi-Omics Approaches to Guide Probiotic Selection to Mitigate Chytridiomycosis and Other Emerging Infectious Diseases. Front Microbiol. 2016; 7: 68. PMID: 26870025, PMCID: PMC4735675, DOI: 10.3389/fmicb.2016.00068.

Woodhams DC, Bell SC, Bigler L, Caprioli RM, Chaurand P, Lam BA, Reinert LK, Stalder U, Vazquez VM, Schliep K, Hertz A, Rollins-Smith LA. Life history linked to immune investment in developing amphibians. Conserv Physiol. 2016; 4(1): cow025. PMID: 27928507, PMCID: PMC5001151, PII: cow025, DOI: 10.1093/conphys/cow025, ISSN: 2051-1434.

Rollins-Smith LA, Fites JS, Reinert LK, Shiakolas AR, Umile TP, Minbiole KP. Immunomodulatory metabolites released by the frog-killing fungus Batrachochytrium dendrobatidis. Infect. Immun [print-electronic]. 2015 Dec; 83(12): 4565-70. PMID: 26371122, PMCID: PMC4645405, PII: IAI.00877-15, DOI: 10.1128/IAI.00877-15, ISSN: 1098-5522.

VanCompernolle S, Smith PB, Bowie JH, Tyler MJ, Unutmaz D, Rollins-Smith LA. Inhibition of HIV infection by caerin 1 antimicrobial peptides. Peptides [print-electronic]. 2015 Sep; 71: 296-303. PMID: 26026377, PII: S0196-9781(15)00160-6, DOI: 10.1016/j.peptides.2015.05.004, ISSN: 1873-5169.

Tatiersky L, Rollins-Smith LA, Lu R, Jardine C, Barker IK, Clark ME, Caswell JL. Effect of glucocorticoids on expression of cutaneous antimicrobial peptides in northern leopard frogs (Lithobates pipiens). BMC Vet. Res. 2015 Aug 8/8/2015; 11: 191. PMID: 26253169, PMCID: PMC4529697, PII: 10.1186/s12917-015-0506-6, DOI: 10.1186/s12917-015-0506-6, ISSN: 1746-6148.

Piovia-Scott J, Pope K, Worth SJ, Rosenblum EB, Poorten T, Refsnider J, Rollins-Smith LA, Reinert LK, Wells HL, Rejmanek D, Lawler S, Foley J. Correlates of virulence in a frog-killing fungal pathogen: evidence from a California amphibian decline. ISME J [print-electronic]. 2015 Jul; 9(7): 1570-8. PMID: 25514536, PMCID: PMC4478697, PII: ismej2014241, DOI: 10.1038/ismej.2014.241, ISSN: 1751-7370.

Rollins-Smith LA, Reinert LK, Burrowes PA. Coqui frogs persist with the deadly chytrid fungus despite a lack of defensive antimicrobial peptides. Dis. Aquat. Org. 2015 Feb 2/10/2015; 113(1): 81-3. PMID: 25667340, DOI: 10.3354/dao02823, ISSN: 0177-5103.

Holden WM, Reinert LK, Hanlon SM, Parris MJ, Rollins-Smith LA. Development of antimicrobial peptide defenses of southern leopard frogs, Rana sphenocephala, against the pathogenic chytrid fungus, Batrachochytrium dendrobatidis. Dev. Comp. Immunol [print-electronic]. 2015 Jan; 48(1): 65-75. PMID: 25218643, PII: S0145-305X(14)00228-6, DOI: 10.1016/j.dci.2014.09.003, ISSN: 1879-0089.

Fites JS, Reinert LK, Chappell TM, Rollins-Smith LA. Inhibition of local immune responses by the frog-killing fungus Batrachochytrium dendrobatidis. Infect. Immun [print-electronic]. 2014 Nov; 82(11): 4698-706. PMID: 25156734, PMCID: PMC4249309, PII: IAI.02231-14, DOI: 10.1128/IAI.02231-14, ISSN: 1098-5522.

McMahon TA, Sears BF, Venesky MD, Bessler SM, Brown JM, Deutsch K, Halstead NT, Lentz G, Tenouri N, Young S, Civitello DJ, Ortega N, Fites JS, Reinert LK, Rollins-Smith LA, Raffel TR, Rohr JR. Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature. 2014 Jul 7/10/2014; 511(7508): 224-7. PMID: 25008531, PMCID: PMC4464781, PII: nature13491, DOI: 10.1038/nature13491, ISSN: 1476-4687.

Holden WM, Ebert AR, Canning PF, Rollins-Smith LA. Evaluation of amphotericin B and chloramphenicol as alternative drugs for treatment of chytridiomycosis and their impacts on innate skin defenses. Appl. Environ. Microbiol [print-electronic]. 2014 Jul; 80(13): 4034-41. PMID: 24771024, PMCID: PMC4054225, PII: AEM.04171-13, DOI: 10.1128/AEM.04171-13, ISSN: 1098-5336.

Groner ML, Rollins-Smith LA, Reinert LK, Hempel J, Bier ME, Relyea RA. Interactive effects of competition and predator cues on immune responses of leopard frogs at metamorphosis. J. Exp. Biol [print-electronic]. 2014 Feb 2/1/2014; 217(Pt 3): 351-8. PMID: 24115058, PII: jeb.091611, DOI: 10.1242/jeb.091611, ISSN: 1477-9145.

Holden WM, Fites JS, Reinert LK, Rollins-Smith LA. Nikkomycin Z is an effective inhibitor of the chytrid fungus linked to global amphibian declines. Fungal Biol [print-electronic]. 2014 Jan; 118(1): 48-60. PMID: 24433676, PII: S1878-6146(13)00154-2, DOI: 10.1016/j.funbio.2013.11.001, ISSN: 1878-6146.

Fites J. Scott. Paralysis of a local immune response by the frog-killing fungus, Batrachochytrium dendrobatidis. Infect. Immun. 2014; 82: 4698-706.

Fites JS, Ramsey JP, Holden WM, Collier SP, Sutherland DM, Reinert LK, Gayek AS, Dermody TS, Aune TM, Oswald-Richter K, Rollins-Smith LA. The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science. 2013 Oct 10/18/2013; 342(6156): 366-9. PMID: 24136969, PMCID: PMC3956111, PII: 342/6156/366, DOI: 10.1126/science.1243316, ISSN: 1095-9203.

Groner ML, Buck JC, Gervasi S, Blaustein AR, Reinert LK, Rollins-Smith LA, Bier ME, Hempel J, Relyea RA. Larval exposure to predator cues alters immune function and response to a fungal pathogen in post-metamorphic wood frogs. Ecol Appl. 2013 Sep; 23(6): 1443-54. PMID: 24147415, ISSN: 1051-0761.

Pask JD, Cary TL, Rollins-Smith LA. Skin peptides protect juvenile leopard frogs (Rana pipiens) against chytridiomycosis. J. Exp. Biol [print-electronic]. 2013 Aug 8/1/2013; 216(Pt 15): 2908-16. PMID: 23580715, PII: jeb.084145, DOI: 10.1242/jeb.084145, ISSN: 1477-9145.

Conlon JM, Reinert LK, Mechkarska M, Prajeep M, Meetani MA, Coquet L, Jouenne T, Hayes MP, Padgett-Flohr G, Rollins-Smith LA. Evaluation of the skin peptide defenses of the Oregon spotted frog Rana pretiosa against infection by the chytrid fungus Batrachochytrium dendrobatidis. J. Chem. Ecol [print-electronic]. 2013 Jun; 39(6): 797-805. PMID: 23653106, DOI: 10.1007/s10886-013-0294-z, ISSN: 1573-1561.

Woodhams DC, Bell SC, Kenyon N, Alford RA, Rollins-Smith LA. Immune evasion or avoidance: fungal skin infection linked to reduced defence peptides in Australian green-eyed treefrogs, Litoria serrata. Fungal Biol [print-electronic]. 2012 Dec; 116(12): 1203-11. PMID: 23245614, PII: S1878-6146(12)00174-2, DOI: 10.1016/j.funbio.2012.10.005, ISSN: 1878-6146.

Gammill WM, Fites JS, Rollins-Smith LA. Norepinephrine depletion of antimicrobial peptides from the skin glands of Xenopus laevis. Dev. Comp. Immunol [print-electronic]. 2012 May; 37(1): 19-27. PMID: 22227319, PII: S0145-305X(11)00326-0, DOI: 10.1016/j.dci.2011.12.012, ISSN: 1879-0089.

Woodhams DC, Geiger CC, Reinert LK, Rollins-Smith LA, Lam B, Harris RN, Briggs CJ, Vredenburg VT, Voyles J. Treatment of amphibians infected with chytrid fungus: learning from failed trials with itraconazole, antimicrobial peptides, bacteria, and heat therapy. Dis. Aquat. Org. 2012 Feb 2/17/2012; 98(1): 11-25. PMID: 22422126, DOI: 10.3354/dao02429, ISSN: 0177-5103.

Becker, M.H., Harris, R.N., Minbiole, K. P.C., Schwantes, C.R., Rollins-Smith, L.A., Reinert, L.K., Brucker, R.M., Domangue, R.J., and Gratwicke, B.. Towards a better understanding of the use of probiotics for preventing chytridiomycosis in Panamanian golden frogs. 2012.

Venesky, M.D., Wilcoxen, T.E., Rensel, M.A., Rollins-Smith, L., Kerby, J.L., and Parris, M.J.. Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog (Lithobates sphenocephalus) tadpoles. 2012.

Pask, J.D., Woodhams, D.C., and Rollins-Smith, L. A.. The ebb and flow of antimicrobial skin peptides defends northern leopard frogs (Rana pipiens) against chytridiomycosis. 2012.

Becker MH, Harris RN, Minbiole KP, Schwantes CR, Rollins-Smith LA, Reinert LK, Brucker RM, Domangue RJ, Gratwicke B. Towards a better understanding of the use of probiotics for preventing chytridiomycosis in Panamanian golden frogs. Ecohealth [print-electronic]. 2011 Dec; 8(4): 501-6. PMID: 22328095, DOI: 10.1007/s10393-012-0743-0, ISSN: 1612-9210.

Rollins-Smith LA, Ramsey JP, Pask JD, Reinert LK, Woodhams DC. Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integr. Comp. Biol [print-electronic]. 2011 Oct; 51(4): 552-62. PMID: 21816807, PII: icr095, DOI: 10.1093/icb/icr095, ISSN: 1557-7023.

Walke, J.B., Harris, R.N., Reinert, L.K., Rollins-Smith, L.A., and Woodhams, D.C.. Social immunity in amphibians: Evidence of vertical transmission of innate defenses. Biotropica. 2011; 43: 396-400.

Ramsey JP, Reinert LK, Harper LK, Woodhams DC, Rollins-Smith LA. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infect. Immun [print-electronic]. 2010 Sep; 78(9): 3981-92. PMID: 20584973, PMCID: PMC2937463, PII: IAI.00402-10, DOI: 10.1128/IAI.00402-10, ISSN: 1098-5522.

Woodhams, D.C., Kenyon, N., Bell, S., Alford, R.A., Chen, S., Billheimer, D., Shyr, Y., and Rollins-Smith, L.A.. Adaptations of skin peptide defences and possible response to the amphibian chytrid fungus in populations of Australian green-eyed treefrogs, Litoria genimaculata. Diversity Distrib. 2010; 16: 703-12.

Tennessen JA, Woodhams DC, Chaurand P, Reinert LK, Billheimer D, Shyr Y, Caprioli RM, Blouin MS, Rollins-Smith LA. Variations in the expressed antimicrobial peptide repertoire of northern leopard frog (Rana pipiens) populations suggest intraspecies differences in resistance to pathogens. Dev. Comp. Immunol [print-electronic]. 2009 Dec; 33(12): 1247-57. PMID: 19622371, PMCID: PMC2927990, PII: S0145-305X(09)00151-7, DOI: 10.1016/j.dci.2009.07.004, ISSN: 1879-0089.

Rollins-Smith LA. The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochim. Biophys. Acta [print-electronic]. 2009 Aug; 1788(8): 1593-9. PMID: 19327341, PII: S0005-2736(09)00079-0, DOI: 10.1016/j.bbamem.2009.03.008, ISSN: 0006-3002.

Rollins-Smith LA, Ramsey JP, Reinert LK, Woodhams DC, Livo LJ, Carey C. Immune defenses of Xenopus laevis against Batrachochytrium dendrobatidis. Front Biosci (Schol Ed). 2009; 1: 68-91. PMID: 19482684, PII: 8, ISSN: 1945-0524.

Abdel-Wahab YH, Power GJ, Flatt PR, Woodhams DC, Rollins-Smith LA, Conlon JM. A peptide of the phylloseptin family from the skin of the frog Hylomantis lemur (Phyllomedusinae) with potent in vitro and in vivo insulin-releasing activity. Peptides [print-electronic]. 2008 Dec; 29(12): 2136-43. PMID: 18848963, PII: S0196-9781(08)00397-5, DOI: 10.1016/j.peptides.2008.09.006, ISSN: 0196-9781.

Gibble RE, Rollins-Smith L, Baer KN. Development of an assay for testing the antimicrobial activity of skin peptides against the amphibian chytrid fungus (Batrachochytrium dendrobatidis) using Xenopus laevis. Ecotoxicol. Environ. Saf [print-electronic]. 2008 Oct; 71(2): 506-13. PMID: 18067960, PII: S0147-6513(07)00256-4, DOI: 10.1016/j.ecoenv.2007.10.016, ISSN: 1090-2414.

Woodhams DC, Kilburn VL, Reinert LK, Voyles J, Medina D, Ibáñez R, Hyatt AD, Boyle DG, Pask JD, Green DM, Rollins-Smith LA. Chytridiomycosis and amphibian population declines continue to spread eastward in Panama. Ecohealth [print-electronic]. 2008 Sep; 5(3): 268-74. PMID: 18807089, DOI: 10.1007/s10393-008-0190-0, ISSN: 1612-9210.

Woodhams DC, Alford RA, Briggs CJ, Johnson M, Rollins-Smith LA. Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology. 2008 Jun; 89(6): 1627-39. PMID: 18589527, ISSN: 0012-9658.

Sheafor B, Davidson EW, Parr L, Rollins-Smith L. Antimicrobial peptide defenses in the salamander, Ambystoma tigrinum, against emerging amphibian pathogens. J. Wildl. Dis. 2008 Apr; 44(2): 226-36. PMID: 18436656, PII: 44/2/226, DOI: 10.7589/0090-3558-44.2.226, ISSN: 0090-3558.

Conlon JM, Woodhams DC, Raza H, Coquet L, Leprince J, Jouenne T, Vaudry H, Rollins-Smith LA. Peptides with differential cytolytic activity from skin secretions of the lemur leaf frog Hylomantis lemur (Hylidae: Phyllomedusinae). Toxicon [print-electronic]. 2007 Sep 9/15/2007; 50(4): 498-506. PMID: 17561225, PII: S0041-0101(07)00162-6, DOI: 10.1016/j.toxicon.2007.04.017, ISSN: 0041-0101.

Davidson C, Benard MF, Shaffer HB, Parker JM, O'Leary C, Conlon JM, Rollins-Smith LA. Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs. Environ. Sci. Technol. 2007 Mar 3/1/2007; 41(5): 1771-6. PMID: 17396672, ISSN: 0013-936X.

Pandelova I, Hewitt SR, Rollins-Smith LA, Hays JB. UVB dose-toxicity thresholds and steady-state DNA-photoproduct levels during chronic irradiation of inbred Xenopus laevis tadpoles. Photochem. Photobiol. 2006 Jul; 82(4): 1080-7. PMID: 17205633, ISSN: 0031-8655.

Woodhams DC, Voyles J, Lips KR, Carey C, Rollins-Smith LA. Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses. J. Wildl. Dis. 2006 Apr; 42(2): 207-18. PMID: 16870844, PII: 42/2/207, DOI: 10.7589/0090-3558-42.2.207, ISSN: 0090-3558.

Rollins-Smith LA, Woodhams DC, Reinert LK, Vredenburg VT, Briggs CJ, Nielsen PF, Conlon JM. Antimicrobial peptide defenses of the mountain yellow-legged frog (Rana muscosa). Dev. Comp. Immunol [print-electronic]. 2006; 30(9): 831-42. PMID: 16330099, PII: S0145-305X(05)00200-4, DOI: 10.1016/j.dci.2005.10.005, ISSN: 0145-305X.

Woodhams DC, Rollins-Smith LA, Carey C, Reinert L, Tyler MJ, Alford RA. Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia [print-electronic]. 2006 Jan; 146(4): 531-40. PMID: 16205955, DOI: 10.1007/s00442-005-0228-8, ISSN: 0029-8549.

VanCompernolle SE, Taylor RJ, Oswald-Richter K, Jiang J, Youree BE, Bowie JH, Tyler MJ, Conlon JM, Wade D, Aiken C, Dermody TS, KewalRamani VN, Rollins-Smith LA, Unutmaz D. Antimicrobial peptides from amphibian skin potently inhibit human immunodeficiency virus infection and transfer of virus from dendritic cells to T cells. J. Virol. 2005 Sep; 79(18): 11598-606. PMID: 16140737, PMCID: PMC1212620, PII: 79/18/11598, DOI: 10.1128/JVI.79.18.11598-11606.2005, ISSN: 0022-538X.

King JD, Rollins-Smith LA, Nielsen PF, John A, Conlon JM. Characterization of a peptide from skin secretions of male specimens of the frog, Leptodactylus fallax that stimulates aggression in male frogs. Peptides [print-electronic]. 2005 Apr; 26(4): 597-601. PMID: 15752573, PII: S0196-9781(04)00491-7, DOI: 10.1016/j.peptides.2004.11.004, ISSN: 0196-9781.

Rollins-Smith LA, King JD, Nielsen PF, Sonnevend A, Conlon JM. An antimicrobial peptide from the skin secretions of the mountain chicken frog Leptodactylus fallax (Anura:Leptodactylidae). Regul. Pept. 2005 Jan 1/15/2005; 124(1-3): 173-8. PMID: 15544856, PII: S0167-0115(04)00246-0, DOI: 10.1016/j.regpep.2004.07.013, ISSN: 0167-0115.

Rollins-Smith LA, Conlon JM. Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Dev. Comp. Immunol [print-electronic]. 2005; 29(7): 589-98. PMID: 15784290, PII: S0145-305X(04)00192-2, DOI: 10.1016/j.dci.2004.11.004, ISSN: 0145-305X.

Rollins-Smith LA, Reinert LK, O'Leary CJ, Houston LE, Woodhams DC. Antimicrobial Peptide defenses in amphibian skin. Integr. Comp. Biol. 2005 Jan; 45(1): 137-42. PMID: 21676754, PII: 45/1/137, DOI: 10.1093/icb/45.1.137, ISSN: 1540-7063.

Rollins-Smith LA, Hopkins BD, Reinert LK. An amphibian model to test the effects of xenobiotic chemicals on development of the hematopoietic system. Environ. Toxicol. Chem. 2004 Dec; 23(12): 2863-7. PMID: 15648761, ISSN: 0730-7268.

Christin, M.S., Menard, L., Gendron, A.D., Ruby, S., Cyr, D., Marcogliese, D., Rollins-Smith, L., and Fournier, M.. Effects of agricultural pesticides on the immune system of Xenopus laevis and Rana pipiens. Aquat. Toxicol. 2004; 67(()): 33-43.

Chinchar, V.G., Bryan, L., Silphadaung, U., Noga, E., Wade, D., and Rollins-Smith, L.. Inactivation of viruses infecting ectothermic animals by amphibian and piscine antimicrobial peptides. Virology. 2004; 323(()): 268-75.

Rollins-Smith LA, Carey C, Conlon JM, Reinert LK, Doersam JK, Bergman T, Silberring J, Lankinen H, Wade D. Activities of temporin family peptides against the chytrid fungus (Batrachochytrium dendrobatidis) associated with global amphibian declines. Antimicrob. Agents Chemother. 2003 Mar; 47(3): 1157-60. PMID: 12604562, PMCID: PMC149293, ISSN: 0066-4804.

Conlon, J.M., Sonnevend, A., Patel, M., Davidson, D., Nielsen, P.F., Pal, T., and Rollins-Smith, L.A.. Isolation of peptides of the brevinin-1 family with potent candidacidal activity from the skin secretions of the frog Rana boylii. J. Pept. Res. 2003; 62: 205-13.

Rollins-Smith LA, Reinert LK, Miera V, Conlon JM. Antimicrobial peptide defenses of the Tarahumara frog, Rana tarahumarae. Biochem. Biophys. Res. Commun. 2002 Sep 9/20/2002; 297(2): 361-7. PMID: 12237127, PII: S0006291X02022179, ISSN: 0006-291X.

Rollins-Smith LA, Carey C, Longcore J, Doersam JK, Boutte A, Bruzgal JE, Conlon JM. Activity of antimicrobial skin peptides from ranid frogs against Batrachochytrium dendrobatidis, the chytrid fungus associated with global amphibian declines. Dev. Comp. Immunol. 2002 Jun; 26(5): 471-9. PMID: 11906726, PII: S0145305X0100088X, ISSN: 0145-305X.

Rollins-Smith LA, Doersam JK, Longcore JE, Taylor SK, Shamblin JC, Carey C, Zasloff MA. Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Dev. Comp. Immunol. 2002 Jan; 26(1): 63-72. PMID: 11687264, PII: S0145305X01000416, ISSN: 0145-305X.

Jeyakumar LH, Ballester L, Cheng DS, McIntyre JO, Chang P, Olivey HE, Rollins-Smith L, Barnett JV, Murray K, Xin HB, Fleischer S. FKBP binding characteristics of cardiac microsomes from diverse vertebrates. Biochem. Biophys. Res. Commun. 2001 Mar 3/9/2001; 281(4): 979-86. PMID: 11237759, PII: S0006-291X(01)94444-4, DOI: 10.1006/bbrc.2001.4444, ISSN: 0006-291X.

2001; Available from: .

Rollins-Smith LA. Neuroendocrine-immune system interactions in amphibians: implications for understanding global amphibian declines. Immunol. Res. 2001; 23(2-3): 273-80. PMID: 11444392, PII: IR:23:2-3:273, DOI: 10.1385/IR:23:2-3:273, ISSN: 0257-277X.

Rollins-Smith LA, Davis AT, Reinert LK. Pituitary involvement in T cell renewal during development and metamorphosis of Xenopus laevis. Brain Behav. Immun. 2000 Sep; 14(3): 185-97. PMID: 10970679, PII: S0889-1591(99)90569-X, DOI: 10.1006/brbi.1999.0569, ISSN: 0889-1591.

Carey, C., Cohen, N., and Rollins-Smith- L. Amphibian Declines: An Immunological Perspective. 1999.

Rollins-Smith LA. Metamorphosis and the amphibian immune system. Immunol. Rev. 1998 Dec; 166: 221-30. PMID: 9914915, ISSN: 0105-2896.

Barker KS, Davis AT, Li B, Rollins-Smith LA. In vitro studies of spontaneous and corticosteroid-induced apoptosis of lymphocyte populations from metamorphosing frogs/RU486 inhibition. Brain Behav. Immun. 1997 Jun; 11(2): 119-31. PMID: 9299061, PII: S0889-1591(97)90489-X, DOI: 10.1006/brbi.1997.0489, ISSN: 0889-1591.

Rollins-Smith LA, Barker KS, Davis AT. Involvement of glucocorticoids in the reorganization of the amphibian immune system at metamorphosis. Dev. Immunol. 1997; 5(2): 145-52. PMID: 9587715, PMCID: PMC2275978, ISSN: 1044-6672.

Rollins-Smith LA, Flajnik MF, Blair PJ, Davis AT, Green WF. Involvement of thyroid hormones in the expression of MHC class I antigens during ontogeny in Xenopus. Dev. Immunol. 1997; 5(2): 133-44. PMID: 9587714, PMCID: PMC2275975, ISSN: 1044-6672.

Rollins-Smith LA, Needham DA, Davis AT, Blair PJ. Late thymectomy in Xenopus tadpoles reveals a population of T cells that persists through metamorphosis. Dev. Comp. Immunol. 1996 May; 20(3): 165-74. PMID: 8955591, PII: 0145305X96000183, ISSN: 0145-305X.

Carlson, D.L., Williams, J.W. III., Rollins-Smith, L.A., Christ, C.G. John, J.C., Williams, C.S., and McKinnell, R.G. Pronephric carcinoma: chromosomes of cells rescued from apoptosis by an oncogenic herpesvirus. J. Comp. Path. 1995; 113: 277-86.

Kinney MC, Hummell DS, Villiger PM, Hourigan A, Rollins-Smith L, Glick AD, Lawton AR. Increased interleukin-6 (IL-6) production in a young child with clinical and pathologic features of multicentric Castleman's disease. J Clin Immunol. 1994 Nov; 14(6): 382-90. PMID: 7883866, DOI: 10.1007/BF01546323, ISSN: 0271-9142.

Carlson, D.L. Sauerbier, W., Rollins-Smith, L,A. and McKinnell, R.G. The presence of DNA sequences of the Lucké herpesvirus in normal and neoplastic kidney tissue of Rana pipiens. J. Comp. Path. 1994; 110: 349-55.

Carlson, D.L., Sauerbier, W., Rollins-Smith, L.A. and McKinnell, R.G. Fate of herpesvirus DNA in embryos and tadpoles cloned from Lucké renal carcinoma nuclei. J. Comp. Path. 1994; 111: 197-203.

Kinney, M.C., Hummell, D.S., Villiger, P.M., Hourigan, A., Rollins-Smith, L.,Glick, A.D., and Lawton, A.R. Increased interleukin-6 (IL-6) production in a young child with clinical and pathologic features of multicentric Castleman's disease. J. Clin. Immunol. 1994; 14: 382-90.

Rollins-Smith LA, Blair PJ. The effects of corticosteroid hormones and thyroid hormones on lymphocyte viability and proliferation during development and metamorphosis of Xenopus laevis. Differentiation. 1993 Oct; 54(3): 155-60. PMID: 8270143, ISSN: 0301-4681.

Rollins-Smith LA, Davis AT, Blair PJ. Effects of thyroid hormone deprivation on immunity in postmetamorphic frogs. Dev. Comp. Immunol. 1993 Mar; 17(2): 157-64. PMID: 8388813, PII: 0145-305X(93)90025-L, ISSN: 0145-305X.

McKinnell, R.G., Lust, J.M., Sauerbier, W., Rolilins-Smith, L.A., Williams, J.W.,III, Williams, C.S., and Carlson, D.L. Genomic plasticity of the Lucké renal carcinoma: a review. Int. J. Dev. Biol. 1993; 37: 213-9.

Rollins-Smith LA, Blair PJ, Davis AT. Thymus ontogeny in frogs: T-cell renewal at metamorphosis. Dev. Immunol. 1992; 2(3): 207-13. PMID: 1320967, PMCID: PMC2275863, ISSN: 1044-6672.

Lust, J.M., Carlson, D.L., Kowles, R., Rollins-Smith, L.A., Williams, J.W., III, and McKinnell, R.G. Allografts of tumor nuclear transplantation embryos: differentiation competence. Proc. Natl. Acad. Sci USA. 1991; 88(()): 6883-7.

Rollins-Smith LA, Parsons SC, Cohen N. Immune responses of intact and embryonically enucleated frogs to self-lens antigens. J. Immunol. 1990 Nov 11/15/1990; 145(10): 3262-7. PMID: 2230117, ISSN: 0022-1767.

Rollins-Smith LA, Blair P. Contribution of ventral blood island mesoderm to hematopoiesis in postmetamorphic and metamorphosis-inhibited Xenopus laevis. Dev. Biol. 1990 Nov; 142(1): 178-83. PMID: 2172056, PII: 0012-1606(90)90161-B, ISSN: 0012-1606.

Rollins-Smith LA, Blair P. Expression of class II major histocompatibility complex antigens on adult T cells in Xenopus is metamorphosis-dependent. Dev. Immunol. 1990; 1(2): 97-104. PMID: 1967017, PMCID: PMC2275827, ISSN: 1044-6672.

Rollins-Smith LA, Parsons SC, Cohen N. Effects of thyroxine-driven precocious metamorphosis on maturation of adult-type allograft rejection responses in early thyroidectomized frogs. Differentiation. 1988 May; 37(3): 180-5. PMID: 3046979, ISSN: 0301-4681.

Rollins-Smith LA, Lawton AR. Regulation of B-cell differentiation: anti-mu antibodies have opposite effects on differentiation stimulated by bacterial lipopolysaccharide and 8-mercaptoguanosine. J. Mol. Cell. Immunol. 1988; 4(1): 9-19. PMID: 3266925, ISSN: 0724-6803.

Rollins-Smith, L.A., Parsons, S.C.V., and Cohen, N. During frog ontogeny, PHA and Con A responsiveness of splenocytes precedes that of thymocytes. Immunology. 1984; 52: 491-500.

Rollins-Sntith, L.A., and Cohen, N. Self-pituitary grafts are not rejected by leopard frogs deprived of their pituitary anlagen as embryos. Nature. 1982; 299: 820-1.

Rollins, L.A. and Cohen, N. On tadpoles, transplantation, and tolerance. Development and Differentiation of Vertebrate Lymphocytes. J. D. Horton (Ed.) Elsevier/North Holland, Amsterdam. 1980; 203-14.