Overview
There is an old saying that "pathology is the mother of medicine." Diseases, and more specifically the discipline of studying diseases (pathology), are why we have medicine and biomedical research. Correctly identifying a disease and the various processes each disease undergoes as it develops is the basis of most work done at The Jackson Laboratory. Through a collaborative effort of scientists in our Jackson Aging Center, we are identifying strain specific diseases in 32 heavily used inbred strains of mice and using modern genetic technologies are mapping the genes responsible for many of these diseases. As humans get similar diseases as they age, this information will be vitally important to studying complex genetic diseases associated with aging.
Alopecia areata, an autoimmune disease featuring hair loss, is a long-term focus of our laboratory group. We have identified four regions of the mouse genome that contain susceptibility genes for alopecia areata and have identified a critical gene in the primary effector cells. We are also characterizing how drug targets change during the development and progression of the disease and are working to make new diagnostic and prognostic tools available to the medical community. We also work on projects investigating chronic proliferative dermatitis and B6 alopecia as well as characterizing mutant mice with hair medulla defects and a new spontaneous mutant with blistering of the skin.
Scientific report
Experimental Dermatology and General Mouse Pathology
Our laboratory's primary interest is the identification and characterization of skin and adnexal diseases in laboratory mice as models for genetically based human skin diseases. However, since our group includes veterinarian and physician scientists, all with broad medical training, we are involved with identifying and defining mouse models for many different types of diseases including inflammatory bowel disease, autoimmune diseases, vascular and lymphatic abnormalities, and many other diseases affecting a variety of organ systems. Our horizons broadened even further when we became a critical part of the new Jackson Aging Center at The Jackson Laboratory.
Alopecia areata is a long-term major focus of our laboratory group. Alopecia areata and its more severe forms, alopecia totalis and universalis, are forms of a cell-mediated autoimmune skin disease that targets actively growing (anagen stage) hair follicles. Building on previous work done with Dr. Lloyd King (Vanderbilt U.) and several Jackson Laboratory Staff Scientists (Drs. Gregory Cox, Gary Churchill, and Renhua Li) in which we identified four quantitative trait loci (QTL) for our C3H/HeJ mouse model of alopecia areata, we used the haplotype in silico mapping approach, with the help of Benjamin King (The Jackson Laboratory), to identify a critical gene in the activation of CD8+ T cells, the primary effector cell. These findings are being confirmed in collaboration with immunologist Dr. Derry Roopenian (The Jackson Laboratory Staff Scientist and Bar Harbor Biotechnology). With funding from the National Alopecia Areata Foundation (NAAF), we set up a preclinical screening system for novel drug efficacy trials at the JAX West facility in West Sacramento, Calif., initially working with Dr. Kara Koehler and now with Dr. Leon Hall. To support this drug screening system, as well as to investigate the fundamental mechanisms involved in onset and progression of alopecia areata, we performed large-scale longitudinal gene expression analysis of our skin graft-induced C3H/HeJ mouse model using the Ingenuity Network Analysis program to identify known drug targets. This is part of Dr. Jing Sun's (The Jackson Laboratory) Ph.D. thesis project. Our results clearly confirmed that drug targets change throughout the development and progression of alopecia areata, indicating that effective treatment requires that specific drugs be used alone or in combination at various stages of the disease. These results help explain the frustration of patients with current treatment options. More importantly, we are identifying a variety of important molecular networks involved in the pathogenesis of alopecia areata. Our findings will help us create alopecia areata-specific molecular assays to provide physicians with more accurate diagnostic and prognostic tools. We are working closely with Dr. Derry Roopenian to develop and make these new tools available to the medical community.
Rosemarie Seymour, D.V.M., a veterinarian working on a Ph.D. through collaboration with the University of Maine in Orono, is studying the genetics and immunologic defects of the chronic proliferative dermatitis mutant mouse (cpdm). These mice develop severe alopecia and scaling due to large numbers of eosinophils in the dermis. Working with Dr. Harm HogenEsch (Purdue U.), we are investigating the cytokine and chemokine pathways in this disease. Previously we found that mutant mice fail to develop Peyer's patches in the intestine and that the secondary lymphoid tissues do not develop properly. Dr. Seymour's work focuses on the pathways involved in normal development of these structures and how this relates to the severe skin and overall systemic effects of this single-gene defect. Dr. Seymour recently identified the mutated gene in the cpdm mouse, and we are currently creating floxed alleles as well as yellow fluorescent protein-expressing transgenic mice to define the biological function of this novel gene in several organs. Drs. Gregory Cox and Leonard Shultz (The Jackson Laboratory) are active partners in this project.
We are also investigating the relatively common forms of hair loss and skin ulcers that arise spontaneously in C57BL/6 (B6) substrains of mice. This disease process is commonly referred to as B6 alopecia, chronic ulcerative dermatitis, or B6 dermatitis, and the severe form results from a primary hair follicle dystrophy. Working with Drs. Helen Everts, David Ong, and Lloyd E. King (all of Vanderbilt U.), we are focusing on abnormal vitamin A metabolism as an underlying mechanism in this disease. Comparative work with Drs. King and Leonard Sperling (Uniformed Services U.) indicates that this may be a new and much needed preclinical model for a form of human cicatrical alopecia.
Dr. Alexander Awgulewitsch (Medical U. South Carolina), an expert in homeobox gene regulation of hair follicle function, approached us to help his group characterize mutant mice with hair medulla defects resulting from overexpression or lack of expression of Hoxc13. Among the genes Hoxc13 interacts with is Foxq1, the gene mutated in satin mice, which also have a hair medulla abnormality. Dr. Baojin Wu, a visiting investigator here for a year from the Medical School of Yangzhou U., Yangzhou Jiangsu, China, recently identified the mutation in a new allelic mutation of satin (MRL/LpJ-Foxq1sa-J). He also recently identified the mutated gene responsible for the spontaneous mutation called hair interior defect (hid), which also has a hair medulla defect. All AKR/J mice are homozygous for this autosomal recessive mutation. Hid is located in an interval with no known genes involved in hair follicle development. We have narrowed our list of candidate genes and these are currently being sequenced. These results are part of a larger project with Dr. Awgulewitsch and his graduate students, Christopher Potter and Nathan Pruett (Medical U. South Carolina), to use hair medulla formation as a paradigm for analyzing gene networks involved in hair follicle differentiation. We have an expanding group of novel and historical mutant strains and stocks with hair medulla defects that involve many different autosomal recessive mutations. These unique tools are critical to define the gene networks involved in normal and abnormal skin and hair biology.
Working with Drs. Derry Roopenian and Jason Bubier (The Jackson Laboratory) we discovered a new spontaneous mutant mouse that results in blistering of the skin, particularly around the ears. It was initially named sore ears for this reason. Abnormalities in the basement membrane indicate that this is a form of junctional epidermolysis bullosa. We are doing comparative studies with Drs. Joe-David Fine and Lloyd E. King, Jr. (Vanderbilt U.). We recently identified the mutated gene and are using the model to identify modifier genes that affect quality and length of life.
Our laboratory provides the pathology infrastructure for the Jackson Aging Center. All mice utilized in this project are brought to us for detailed physiologic and pathologic phenotyping, which includes designing and coordinating numerous ancillary studies with scientists in-house and around the world. We coordinate our work with Drs. David Harrison and Beverly Paigen (The Jackson Laboratory). Histopathology results and disease frequency are posted on the Mouse Phenome Database and Mouse Tumor Biology Database (with Drs. Janan Eppig and Dale Begley, The Jackson Laboratory). These data are also included in Pathbase (with Dr. Paul Schofield, Cambridge U., Cambridge, UK), a mouse pathology database that integrates the expertise of many mouse pathologists to make public annotated images of all diseases in laboratory mice. These data will be part of a large-scale haplotype mapping project to identify genes responsible for chronic debilitating spontaneous diseases. We are also collaborating with Dr. Paul Schofield (Cambridge U.) and Beth Sundberg (The Jackson Laboratory) to expand Pathbase by developing a subdirectory, Skinbase, that describes mutant mice with skin, hair, and nail abnormalities, including information on normal anatomic structures, coordinated with the assistance of a medical specialist to use terms familiar to both veterinarians and physicians.
Training programs for veterinarians and physicians interested in mouse research and pathology continue both here at The Jackson Laboratory as well as off campus. Dr. Thomas Chase, working in Dr. Leonard Shultz's laboratory, is currently on our NIH T32 training grant for veterinarians. Dr. Seymour (see above) completed her work on the T32 training grant and was awarded an NIH K08 Mentored Clinical Scientist grant. Our annual week-long training course for pathologists (Pathology of Mouse Models for Human Diseases) was held this year at the Fred Hutchinson Cancer Center in Seattle and will be held at The Jackson Laboratory in September 2007. Dr. Sundberg conducted a series of minicourses on mouse pathology and mouse databases at Northwestern U., Purdue U., the University of Illinois, and many others are being planned.
Lab staff
Principal Investigator: John P. Sundberg, D.V.M., Ph.D., Diplomate, A.C.V.P.
Research Scientist: Rosemarie E. Seymour, D.V.M., Ph.D.
Research Assistant III: Kathleen Silva
Laboratory Technician III: Vicki Kennedy
Software Engineer I: Beth A. Sundberg, B.A., M.S.
Visiting Investigators: André Bleich, D.V.M., Ph.D., Institut für Versuchstierkunde und Zentrales Tierlaboratorium der Medizinischen Hochschule Hannover, Hannover, Germany, Helen Everts, Ph.D., Department of Biochemistry, Vanderbilt University Medical Center, Nashville, Tenn., Robert Hackman, M.D., Departments of Pathology and Laboratory Medicine, Fred Hutchinson Cancer Research Center, University of Washington, Seattle, Wash., Harm HogenEsch, D.V.M., Ph.D., Dipl. A.C.V.P., Department of Veterinary Pathobiology, Purdue University, West Lafayette, Ind., Herbert C. Morse III, M.D., Chief, Laboratory of Immunopathology, National Institute of Allergy and Infectious Diseases, Bethesda, Md., Paul N. Schofield, Ph.D., Department of Anatomy, University of Cambridge, Cambridge, U.K., Douglas Taylor, D.V.M., Unit for Laboratory Animal Medicine, University of Michigan, Ann Arbor, Mich., Yun You, Ph.D., Mammalian Genetics and Genomics Group, Life Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tenn.
Research Administrative Assistant: Maxine Friend
Publication listings
Sundberg JP, Silva KA, Zhang W, Sundberg BA, Edwards K, King LE, Davis RL, Black S. 2009. Recombinant human hepatitis B vaccine initiating alopecia areata: testing the hypothesis using the C3H/HeJ mouse model. Vet Dermatol. (Epub ahead of print).
Ghim S, Jenson AB, Bubier JA, Silva KA, Smith RS, Sundberg JP. 2008. Cataracts in transgenic mice caused by a human papillomavirus type 18 E7 oncogene driven by KRTI-14. Exp Mol Pathol. 85:77-82.
Sundberg JP, Sundberg BA, Scholfield P. 2008. Integrating mouse anatomy and pathology ontologies into a phenotyping database: Tools for data capture and training. Mamm Genome 19:413-419.
Sun J, Silva KA, McElwee KJ, King LE Jr, Sundberg JP. 2008. The C3H/HeJ mouse and DEBR rat models for alopecia areata: review of preclinical drug screening approaches and results. Exp Dermatol. 17:793-805.
Schofield PN, Brown SD, Sundberg JP, Arends M, Warren MV, Dubus P, Ellender M, Fiette L, Rozell B, Quintanilla-Martinez L, Raspa M, Song JY, van der Valk M, McKerlie C. 2008. PRIME importance of pathology expertise. Nat Biotechnol. 27:24-25.
Rehg JE, Sundberg JP. 2008. Utility of anti-Pax5 in the diagnosis of lymphoproliferative disorders and neoplasia in mice. Comp Med. 58:246-252.
Pruett ND, Visconti RP, Jacobs DF, Scholz D, McQuinn T, Sundberg JP, Awgulewitsch A. 2008. Evidence for Hox-specified positional identities in adult vasculature. BMC Dev Biol. 80:-93.
Mentzer SE, Sundberg JP, Awgulewitsch A, Chao HH, Carpenter DA, Zhang WD, Rinchik EM, You Y. 2008. The mouse hairy ears mutation exhibits an extended growth (anagen) phase in hair follicles and altered Hoxc gene expression in the ears. Vet Dermatol. 19:358-367.
Krupte DM, Begley DA, Sundberg JP, Bult CJ, Eppig JT. 2008. The Mouse Tumor Biology database. Nat Res Cancer. 8:459-465.
King LE, McElwee KJ, Sundberg JP. 2008. Alopecia areata. Curr Dir Autoimmun. 10:280-312.
Ghim S, Jenson AB, Bubier JA, Silva KA, Smith RS, Sundberg JP. 2008. Cataracts in transgenic mice caused by a human papillomavirus type a8 E7 oncogene driven by KRT1-14. Exp Mol Pathol. 85:77-82.
Fantauzzo KA, Tadin-Strapps M, You Y, Mentzer SE, Baumeister FA, Cianfarani S, Van Maldergem L, Warburton D, Sundberg JP, Christiano AM. 2008. A position effect on TRPS1 is associated with Ambras syndrome in humans and hte Koala phenotype in mice. Hum Mol Genet. 17:3539-3551.
Chen J, Jaeger K, Den Z, Koch PJ, Sundberg JP, Roop DR. 2008. Mice expressing a mutant Krt75 (K6hf) allele develop hair and nail defects resembling pachyonychia congenita. J Invest Dermatol. 128:270-279.
Bleich A, Kirsch P, Sahly H, Fahey J, Smoczek A, Hedrich, HJ, Sundberg JP. 2008. Klebsiella oxytoca: opportunistic infections in laboratory rodents. Laboratory Animals. 42:369-375.
Bleich A, Sundberg JP. Smoczek A, von Wasielewski R, de Buhr MF, Janus LM, Julga G, Ukena SN, Hedrich HJ, Gunzer F. 2008. Sensitivity to Escherichia coli Nissle 1917 in mice is dependent on environment and genetic background. Int J Exp Pathol. 89:45-54.
Barthold SW, Borowsky AD, Brayton C, Bronson R, Cardiff RD, Griffey SM, Ince TA, Nikitin AY, Sundberg JP, Valli VE, Ward JM. 2007. From whence will they come? - A perspective on the acute shortage of pathologists in biomedical research. J Vet Diagn Invest 19:455-456.
Seymour RE, Hasham MG, Cox GA, Shultz LD, Hogenesch H, Roopenian DC and Sundberg JP. 2007. Spontaneous mutations in the mouse Sharpin gene result in multiorgan inflammation, immune system dysregulation and dermatitis. Genes Immun. 8:416-421.
Stranges PB, Watson J, Cooper CJ, Choisy-Rossi CM, Stonebraker AC, Beighton RA, Hartig H, Sundberg JP, Servick S, Kaufmann G, Fink PJ and Chervonsky AV. 2007. Elimination of antigen-presenting cells and autoreactive T cells by fas contributes to prevention of autoimmunity. Immunity 26:629-641.
Sundberg JP, Hackman RC, HogenEsch H, Nikitin AY and Ward JM. 2007. Training mouse pathologists: five years of pathology of mouse models of human disease workshops. Toxicol Pathol 35:447-448.
Rector A, Lemey P, Tachezy R, Mostmans S, Ghim SJ, van Doorslaer K, Roelke M, Bush M, Montali RJ, Joslin J, Burk RD, Jenson AB, Sundberg JP, Shapiro B and van Ranst M. 2007. Ancient papillomavirus-host co-speciation in Felidae. Genome Biol 8:R57.
van Doorslaer K, Rector A, Jenson AB, Sundberg JP, van Ranst M and Ghim SJ. 2007. Complete genomic characterization of a murine papillomavirus isolated from papillomatous lesions of a European harvest mouse (Micromys minutus). J Gen Virol 88:1484-1488.
Everts HB, Sundberg JP, King LE, Jr and Ong DE. 2007. Immunolocalization of enzymes, binding proteins, and receptors sufficient for retinoic acid synthesis and signaling during the hair cycle. J Invest Dermatol 127:1593-1604.
Liu Y, Das S, O(lszewski RE, Carpenter DA, Culiat CT, Sundberg JP, Soteropoulos P, Liu X, Doktycz MJ, Michaud EJ and Voy BH. 2007. The near-naked hairless (HrN) mutation disrupts hair formation but is not due to a mutation in the Hairless coding region. J Invest Dermatol 127:1605-1614.
Siebenhaar F, Sharov AA, Peters EM, Sharova TY, Syska W, Mardaryev AN, Freyschmidt-Paul P, Sundberg JP, Maurer M and Botchkarev VA. 2007. Substance P as an immunomodulatory neuropeptide in a mouse model for autoimmune hair loss (alopecia areata). J Invest Dermatol 127:1489-1497.
Sundberg JP, Silva KA, Edwards K, Black S, Jenson AB, King LE. 2007. Failure to induce alopecia areata in C3H/HeJ mice with exogenous interferon gamma. J Exp Anim Sci 43:265-270.
Begley DA, Krupke DM, Vincent MJ, Sundberg JP, Bult CJ and Eppig JT. 2007. Mouse Tumor Biology Database (MTB): status update and future directions. Nucleic Acids Res 35:D638-642.
Mikaelian I, Hovick M, Silva KA, Burzenski LM, Shultz LD, Ackert-Bicknell CL, Cox GA, Sundberg JP. 2006. Expression of terminal differentiation proteins defines stages of mouse mammary gland development. Vet Pathol 43:36-49.
Hogenesch H, Dunham A, Seymour R, Renninger M, Sundberg JP. 2006. Expression of chitinase-like proteins in the skin of chronic proliferative dermatitis (cpdm/cpdm) mice. Exp Dermatol 15:808-814.
Freyschmidt-Paul P, McElwee KJ, Hoffmann R, Sundberg JP, Vitacolonna M, Kissling S, Zoller M. 2006. Interferon-gamma-deficient mice are resistant to the development of alopecia areata. Br J Dermatol 155:515-521.
Lee JW, Beebe K, Nangle LA, Jang J, Longo-Guess CM, Cook SA, Davisson MT, Sundberg JP, Schimmel P, Ackerman SL. 2006. Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443:50-55.
Seymour R, Sundberg JP, Hogenesch H. 2006. Abnormal lymphoid organ development in immunodeficient mutant mice. Vet Pathol 43:401-423.
Potter CS, Peterson RL, Barth JL, Pruett ND, Jacobs DF, Kern MJ, Argraves WS, Sundberg JP, Awgulewitsch A. 2006. Evidence that the satin hair mutant gene Foxq1 is among multiple and functionally diverse regulatory targets for Hoxc13 during hair follicle differentiation. J Biol Chem 281:29245-29255.
Gould DB, Phalan FC, van Mil SE, Sundberg JP, Vahedi K, Massin P, Bousser MG, Heutink P, Miner JH, Tournier-Lasserve E, John SW. 2006. Role of Col4A1 in small-vessel disease and hemorrhagic stroke. N Engl J Med 354:1489-1496.
Bikle DD, Elalieh H, Chang S, Xie Z, Sundberg JP. 2006. Development and progression of alopecia in the vitamin D receptor null mouse. J Cell Physiol 207:340-353.
Books, Book Chapters, and Reviews:
Smith RS, Nishina PM, Sundberg JP, Zwaan J, John SWM. 2007. Eye Research. In: The mouse in biomedical research, Vol 3, Fox J, Newcomer C, Smith A, Barthold S, Quimby F, Davisson M (eds), Elsevier, San Diego, CA, pp 595-615.
Chuong CM, Sundberg JP. 2007. Mouse skin ectodermal organs. In: The Mouse in Biomecial Research, Vol 3, Fox J, Newcomer C, Smith A, Barthold S, Quimby F, Davisson M (eds), Elsevier, San Diego, CA, pp 691-730.
Bult CJ, Krupke CM, Vincent MJ, Allio T, Sundberg JP, Mikaelian I, Eppig JT. 2006. The mouse tumor biology database: an online resource for mouse models of human cancer. In: Cancer Bioinformatics: From therapy design to treatment, Nagl S (ed), John Wiley & Sons Ltd, West Sussex, England, pp 143-153.
Sundberg JP, Ichiki T. 2005. Handbook on Genetically Engineered Mice. CRC Press, Boca Raton, FL.
Schofield PN, Bard JBL, Rozell B, Sundberg JP. 2005. Computational Pathology: challenges in the informatics of phenotype description in mutant mice. In: Handbook on Genetically Engineered Mice, Sundberg JP and Ichiki T (eds), CRC Press, Boca Raton, FL, pp 61-82.
Sundberg JP, Bult C. 2005. Professional use of mutant laboratory mice in research. In: Handbook on Genetically Engineered Mice, Sundberg JP and Ichiki T (eds), CRC Press, Boca Raton, FL, pp 185-210.
Sundberg JP, Ichiki T. 2005. Common diseases found in inbred strains. In: Handbook on Genetically Engineered Mice, Sundberg JP and Ichiki T (eds), CRC Press, Boca Raton, FL, pp223-232.
Sundberg JP, Ichiki T. 2005. Phenotyping postpartum mutant laboratory mice and determining their value as animal models for human diseases. In: Handbook on Genetically Engineered Mice, Sundberg JP and Ichiki T (eds), . CRC Press, Boca Raton, FL, pp 211-222.
Sundberg JP, Ichiki T, Rozell B, Ward JM. 2005. Genetically engineered mice: past, present, and future. In: Handbook on Genetically Engineered Mice, Sundberg JP and Ichiki T (eds), CRC Press, Boca Raton, FL, pp 1-10.
Goldsmith C-AW, Ringwald M, Sundberg JP, Bult CJ, Eppig JT. 2005. Mouse genome informatics: database access to integrated phenotype data. In: Handbook on Genetically Engineered Mice, Sundberg JP and Ichiki T (eds), CRC Press, Boca Raton, FL, pp 39-56.
Sundberg JP, McElwee KJ, King LE. 2004. Spontaneous and experimental skin-graft-transfer mouse models for alopecia areata. In: Animal Models of Human Inflammatory Skin Diseases, Chen LS (ed), CRC Press, Boca Raton, FL, pp435-455.
Sundberg JP. 2004. Skin and Adnexa of the Laboratory Mouse. In: Handbook of Experimental Animals: The Laboratory Mouse, Hedrich HJ (ed), Academic Press, London, pp 195-206.
Seymour RE, Ichiki T, Mikaelian I, Boggess D, Silva KA, Sundberg JP. 2004. Necropsy methods. In: Handbook of Experimental Animals: The Laboratory Mouse. Hedrich HJ (ed), Academic Press, London, pp 495-516.
Mikaelian I, Ichiki T, Ward JM, Sundberg JP. 2004. Diversity of spontaneous neoplasms in commonly used inbred strains and stocks of laboratory mice. In: Handbook of Experimental Animals: The Laboratory Mouse, Hedrich HJ (ed), Academic Press, London, pp 345-354.
Boggess D, Silva KA, Landel C, Mobraaten L, Sundberg JP. 2004. Approaches to handling, breeding, strain preservation, genotyping, and drug administration for mouse models of cancer. In: Mouse Models of Human Cancer, Holland EC (ed), John Wiley & Sons, Inc, Hoboken, NJ, pp 1-14.
Freyschmidt-Paul, McElwee KJ, Happle R, Kissling S, Wenzel E, Sundberg JP, Zoller M, Hoffman R. 2003. Treatment and induction studies in C3H/HeJ mice indicate that interleukin-10 has no immunosuppressive effect on alopecia areata. In: Hair Science and Technology. Van Neste D (ed), Skinterface, Tournai, Belgium, pp 445-459.
Sundberg JP, Bult C. 2003. The professional use of mice in hair follicle research. In: The Biology of the Hair Follicle. Paus R, (ed). R.G. Landes Company, Austin, Texas, in press.
Sundberg JP, McElwee KJ, King LE. 2003. Mouse models for alopecia areata. In: Animal Models of Human Inflammatory Skin Diseases. Chen LS, (ed). CRC Press LLC, Boca Raton, Fla., in press.
Sundberg JP. 2003. Skin and Adnexa of the Laboratory Mouse. In: Handbook of Experimental Animals: The Laboratory Mouse. Hedrich HJ, (ed). Academic Press, London, in press.
Seymour RE, Ichiki T, Mikaelian I, Boggess D, Silva KA, Sundberg JP. 2003. Necropsy methods. In: Handbook of Experimental Animals: The Laboratory Mouse. Hedrich HJ, (ed). Academic Press, London, in press.
Mikaelian I, Ichiki T, Ward JM, Sundberg JP. 2003. Diversity of spontaneous neoplasms in commonly used inbred strains and stocks of laboratory mice. In: Handbook of Experimental Animals: The Laboratory Mouse. Hedrich HJ, (ed). Academic Press, London, in press.
Smith RS, John SWM, Nishina PM, Sundberg JP. 2002. Systematic Evaluation of the Mouse Eye: Anatomy, Pathology, and Biomethods. CRC Press, Boca Raton, Fla.
Smith RS, Sundberg JP, John SWM. 2002. The anterior segment. In: Systematic Evaluation of the Mouse Eye: Anatomy, Pathology, and Biomethods, Smith RS, John SWM, Nishina PM, Sundberg JP, (eds). CRC Press LLC, Boca Raton, Fla., pp. 111-159.
Smith RS, Sundberg JP. Strain background disease characteristics. 2002. In: Systematic Evaluation of the Mouse Eye: Anatomy, Pathology, and Biomethods, Smith RS, John SWM, Nishina PM, Sundberg JP, (eds). CRC Press LLC, Boca Raton, Fla., pp. 67-75.
Sundberg JP, Smith RS, John SWM. 2002. Selection of controls. In: Systematic Evaluation of the Mouse Eye: Anatomy, Pathology, and Biomethods, Smith RS, John SWM, Nishina PM, Sundberg JP, (eds). CRC Press LLC, Boca Raton, Fla., pp. 77-80.
Smith RS, Sundberg JP, John S. 2002. The anterior segment and ocular adnexae. In: Systematic Evaluation of the Mouse Eye: Anatomy, Pathology, and Biomethods. Smith RS, John SWM, Nishina PM, Sundberg JP, (eds). CRC Press LLC, Boca Raton, FL, pp. 3-23.
Smith RS, John SWM, Sundberg JP. 2002. Optic nerve and orbit. In: Systematic Evaluation of the Mouse Eye: Anatomy, Pathology, and Biomethods, Smith RS, John SWM, Nishina PM, Sundberg JP, (eds). CRC Press LLC, Boca Raton, Fla. pp. 227-247.
Smith RS, Hawes NL, Miller J, Sundberg JP, John SWM. 2002. Photography and necropsy. In: Systematic Evaluation of the Mouse Eye: Anatomy, Pathology, and Biomethods, Smith RS, John SWM, Nishina PM, Sundberg JP, (eds). CRC Press LLC, Boca Raton, Fla, pp. 251-264.
Smith RS, Zabaleta A, John SWM, Bechtold LS, Ikeda S, Relyea MJ, Sundberg JP, Liu C-Y, Kao W-Y. 2002. General and special histopathology. In: Systematic Evaluation of the Mouse Eye: Anatomy, Pathology, and Biomethods. Smith RS, John SWM, Nishina PM, Sundberg JP, (eds), CRC Press LLC, Boca Raton, Fla., pp. 265-297.
Ikeda S, Relyea MJ, Sundberg JP. 2002. Immunohistochemistry. In: Systematic Evaluation of the Mouse Eye: Anatomy, Pathology, and Biomethods. Smith RS, John SWM, Nishina PM, Sundberg JP, (eds). CRC Press LLC, Boca Raton, Fla., pp. 277-284
