Systems biology of stem cells; genetic and genomic approaches to human developmental disease
1978 Phi Beta Kappa, Reed College Chapter
1978-1981 Graduate Fellowship, National Science Foundation
1981-1982 Graduate Opportunity Fellowship, University of California
1988 Postdoctoral Fellowship, Muscular Dystrophy Association
1989-1990 Postdoctoral Fellowship, National Institutes of Health NRSA
1993-1996 Basil O'Connor Starter Scholar Research Award, March of Dimes Birth Defects Foundation
2008-Present Co-Director, Cornelia de Lange Foundation Center of Excellence in Research, UC Irvine
2016 RARE Champion of Hope in Science Award, Global Genes Alliance in Rare Diseases
1985-1987 Postdoctoral Associate
Columbia Univ. CP & S, New York, NY
1987 Assistant Instructor
Molecular Embryology of the Mouse course
Cold Spring Harbor Laboratory
Cold Spring Harbor, NY
1987-1990 Postdoctoral Research Associate/Instructor
Tufts Univ. Sch. Med., Boston, MA
1991-1995 Assistant Professor
Department of Biological Sciences
University of Iowa, Iowa City, IA
1995-Present Assistant, Associate, Full Professor (Full Professor 07/2005)
Department of Anatomy & Neurobiology
Univ. Calif., Irvine, Irvine, CA
The overall goal of my laboratory’s research is to understand how changes in cell lineage progression parameters and in the expression of diverse genes act in concert to direct normal development and, when development goes awry, to cause syndromic and non-syndromic birth defects. We are particularly interested in the nervous system, but we also study other systems such as heart, limb, visceral organs, and craniofacial structures. In many of our studies, we use mouse and zebrafish models of Nipbl-deficiency (the major cause of Cornelia de Lange Syndrome (CdLS)) as systems with which to understand this question – a question that is common to many ”transcriptomopathies” that are characterized by global dysregulation of gene expression arising as a consequence of an initial genetic lesion (e.g. Nipbl haploinsufficiency in CdLS, trisomy in Down Syndrome, MECP2 mutation in Rett Syndrome, etc.). Our goals are (1) to gain insight into general principles of developmental regulation by studying animal models of Nipbl-deficiency, and (2) to use these model systems to test therapeutic interventions for CdLS. Our studies on CdLS involve, in addition to me and the members of my laboratory, other investigators at UCI and around the world. Our colleagues at UCI include Arthur Lander, Thomas Schilling (who oversees the work on zebrafish that we pursue as part of our studies of CdLS), and Kyoko Yokomori (whose primary interest in CdLS is in chromatin structure and regulation of gene expression). The papers resulting from such studies are published collaboratively, with between two and four PIs and different members of the various laboratories taking authorships, as appropriate for a given study. My lab’s most recent studies of Nipbl-deficient mice have led to novel insights into the determinants of risk for the development of congenital heart disease (see Santos et al., 2016, PLoS Biology; and review by Gelb BD (The Hole and the Whole: Lessons from Manipulation of Nipbl Deficiency. PLoS Biol. 2016 Sep 8;14(9):e2000494. doi:0.1371/journal.pbio.2000494).
In addition to molecular approaches to studying development and congenital disease, I have increasingly employed a systems biology approach in my laboratory’s studies. I serve as a Theme Leader in Control of Growth and Morphogenesis at UCI’s Center for Complex Biological Systems, a NIGMS-sponsored National Center for Systems Biology. In this capacity, I work with many investigators on interdisciplinary research projects that integrate computational modeling, genomics, and high-throughput data gathering integrated with experimental developmental biology and genetics. My lab’s research in this area has mainly been focused on understanding how signaling systems participate in feedback regulation of stem and progenitor cells and the effects of such feedback on morphogenesis, patterning, and regulated growth of different tissues. The systems for which our contributions have been most significant are the olfactory epithelium, neural retina, and gustatory epithelium of the tongue, although we currently have a project to study neocortex as well. During the review period, we have published a number of studies that combine wet-bench experimentation with extensive mathematical analysis and computational modeling, as well as some papers that are purely theoretical. These studies are published collaboratively, with multiple PIs and members of the participating research groups taking authorships as appropriate for a given study. Our most recent work, published in 2016 in PLoS Computational Biology, is a theoretical exploration of the ways in which feedback effects on stem cell self-renewal can serve as a driving force in morphogenesis (Kunche et al., 2016, PLoS Computational Biology).
Crestina L. Beites, Shimako Kawauchi, Rosaysela Santos, Kimberly K. Gokoffski, and Anne L. Calof (2017) Patterning, cell specification and feedback in the olfactory epithelium. In: Reference Module in Neuroscience and Biobehavioral Psychology, Elsevier, 2017, ISBN 978-0-12-809324-5,http://dx.doi.org/10.1016/XXXXXXXXX, (http://www.sciencedirect.com/science/article/pii/XXXXXXXXXX), In Press.
Newkirk, D., Y.-Y. Chen, R. Chien, W. Zeng, J. Biesinger, E. Flowers, S. Kawauchi, R. Santos, A.L. Calof, A.D. Lander, X. Xie, K. Yokomori (2017) The effect of Nipped-B-like (Nipbl) haploinsufficiency on genome-wide cohesin binding and target gene expression: modeling Cornelia de Lange Syndrome. Clinical Epigenetics, In Press.
Santos R., S. Kawauchi, R.E. Jacobs, M.E. Lopez-Burks, H. Choi, J. Wikenheiser, B., Hallgrimsson, H.A. Jamniczky, S.E. Fraser, A.D. Lander, and A.L. Calof* (2016) Conditional creation and rescue of Nipbl-deficiency in mice reveals multiple determinants of risk for congenital heart defects. PLOS Biology, 14, e2000197. doi: 10.1371/journal.pbio.2000197. PMID: 27606604. * corresponding author ** Reviewed in: PLoS Biology Primer by B. Gelb (2016)“The Hole and the Whole: Lessons from Manipulation of Nipbl Deficiency” 2016 PLoS Biology, and Arney K (2016) “Squeezing the Heart” In: Biomedical Picture of the Day (BPoD),bpod.mrc.ac.uk/archive/2016/10/13
Lopez-Burks, M.E., R. Santos, S. Kawauchi, A.L. Calof and A.D. Lander (2016) Genetic enhancement of limb defects in a mouse model of Cornelia de Lange Syndrome. Am J Med Genet C Semin Med Genet. 2016 Jun;172(2):146-54. doi: 10.1002/ajmg.c.31491. PMID: 27120109.
Kawauchi, S., R. Santos, A. Muto, M.E. Lopez-Burks, T.F. Schilling, A.D. Lander and A.L. Calof (2016) Using Mouse and Zebrafish Models to Understand the Etiology of Developmental Defects in Cornelia de Lange Syndrome. Am J Med Genet C Semin Med Genet. 172(2):138-45. doi: 10.1002/ajmg.c.31484. PMID: 27120001.
Kunche, S., H. Yan, A.L. Calof*, J.S. Lowengrub and A.D. Lander (2016) Feedback, lineages and self-organizing morphogenesis. PLoS Computational Biol, 12, e1004814. doi:10.1371/journal.pcbi.1004814. * corresponding author ** Cited in PLoS Collections, Editor’s Picks in Stem Cell Research (http://collections.plos.org/stem-cell-research).
Chiang M, Hallman S, Cinquin A, de Mochel NR, Paz A, Kawauchi S, Calof AL, Cho KW, Fowlkes CC, Cinquin O. (2015) Analysis of in vivo single cell behavior by high throughput, human-in-the-loop segmentation of three-dimensional images. BMC Bioinformatics 16:397. https://doi.org/10.1186/s12859-015-0814-7 PMID: 26607933, PMCID: PMC4659165.
Muto, A., S. Ikeda, M.E. Lopez-Burks, Y Kikuchi, A.L. Calof*, A.D. Lander and T.F. Schilling (2014) Nipbl and Mediator Cooperatively Regulate Gene Expression to Control Limb Development. PLoS Genetics, 10(9):e1004671. doi: 10.1371/journal.pgen.1004671. PMID 25255084. PMCID: PMC4177752. * corresponding author
S. Remeseiro, A. Cuadrado, S. Kawauchi, A.L. Calof, A.D. Lander and A. Losada (2013) Reduction of Nipbl impairs cohesin loading locally and affects transcription but not cohesion-dependent functions in a mouse model of Cornelia de Lange Syndrome. Biochim Biophys Acta 1832, 2097-102. doi: 10.1016/j.bbadis.2013.07.020. PMCID: PMC3825806.
Kawauchi S, Santos R, Kim J, Wu, HH, Gokoffski KK, Lander AD and Calof AL (2012) Genetic interactions of cell intrinsic factors and secreted signals regulate neurogenesis in olfactory epithelium. Journal for the Japanese Association for Study of Taste and Smell 19(1): 49-55. (in Japanese)
Lander AD, Kimble J, Clevers H, Fuchs E, Montarras D, Buckingham M, Calof AL, Trumpp A, and Oskarsson T (2012) What does the concept of the stem cell niche really mean today? BMC Biology, 10, 19: pp 1-15; doi: 10.1186/1741-7007-10-19.
Santos R, Wu H-H, Hamilton J, Pinter R, Hindges R & Calof, AL (2012) Restoration of retinal development in Vsx2 deficient mice by reduction of Gdf11 activity. Adv. Exp. Med. Biol. 723: 671-677. PMID 22183392
Muto A, Calof AL, Lander AD, and Schilling, T.F. (2011) Multifactoral origins of heart and gut defects in nipbl-deficient zebrafish, a model of Cornelia de Lange Syndrome. PLoS Biology Oct;9(10):e1001181. Epub 2011 Oct 25. (comment: PLoS Biol. 2011 Oct;9(10):e1001180) PMCID: PMC3201921. ** Reviewed in J. Weaver (2011) “Genetic Origins of Birth Defects Revealed by New Animal Model”, PLoS Biology, (http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.1001180).
Gokoffski K, Wu H-H, Beites CL, Kim J, Kim E, Matzuk MM, Johnson JE, Lander AD & Calof AL (2011) Activin and GDF11 collaborate in feedback control of neuroepithelial stem cell proliferation and fate. Development, 138: pp. 4131-4142.
Chien R, Zeng W, Kawauchi S, Santos R, Gregson HC, Schmiesing JA, Newkirk D, Kong X, Ball AR J, Calof AL, Lander AD, Groudine M & Yokomori K (2011) Cohesin mediates chromatin interactions that regulate mammalian beta-globin expression. J. Biol. Chem. 286:DOI 10.1074.
Gokoffski, K.K., Kawauchi, S., H.-H. Wu, R. Santos, P.W.L. Hollenbeck, A.D. Lander and A.L. Calof (2010) "Feedback regulation of neurogenesis in the mammalian olfactory epithelium: New insights from genetics and systems biology." In: Neurobiology of Olfaction, (A. Menini, Ed.) CRC Press, pp. 241-265. PMID:21882434.
Chou, C.-S., Lo, W.-C., Gokoffski, K.K., Zhang, Y.-T., Wan, F.Y.M., Lander, A.D., Calof, A.L., and Nie, Q. (2010) Spatial dynamics of multistage cell lineages in tissue stratification. Biophys. J. 99 (10): 3145-3154.
Beites, C.L., Kawauchi, S., & Calof, A.L. (2009) Olfactory neuron patterning and specification. In: Developmental Neurobiology (G. Lemke, Ed.) Elsevier, Oxford, pp. 226-237.
Beites, C.L., Kawauchi, S., & Calof, A.L. (2009) Olfactory neuron patterning and specification. In: The New Encyclopedia of Neuroscience, Vol. 7 (L. Zipusky, Ed.) Elsevier, Oxford, pp. 145-156.
Kawauchi, S, Santos, R, Kim, J, Hollenbeck, PLW, Murray, RC, and Calof, AL (2009) The role of Foxg1 in the development of neural stem cells of the olfactory epithelium. Ann. NY Acad. Sci., 1170: 21-27
Barlow, LA and Calof, AL (2009) Stem cells in sensory epithelium development and regeneration. Ann. NY Acad. Sci., 1170: 5-6.
Kawauchi, S, Calof, AL**, Santos, R., Lopez-Burks, ME, Young, CM, Hoang, MP, Chua, A., Lao, T., Lechner, MS, Daniel, JA, Nussenzweig, A., Kitzes, L., Yokomori, K., Hallgrimsson, B. and Lander, A.D. (2009) Multiple organ system defects and transcriptional dysregulation in a mouse model of Cornelia de Lange Syndrome. PLoS Genetics 5(9): e1000650. Doi:10.1371/journal.pgen.1000650. (** = Co-first author as well as corresponding author)
Beites, CL, Hollenbeck, PLW, Kim, J, Lovell-Badge, R, Lander, AD, and Calof, AL (2009) Follistatin modulates a BMP autoregulatory loop to control size and patterning of sensory domains in the developing tongue. Development, 136: 2187-2197.
Kawauchi, S., Kim, J., Santos, R., Wu, H. H., Lander, A. D. and Calof, A. L. (2009). Foxg1 promotes olfactory neurogenesis by antagonizing Gdf11. Development 136, 1453-64.
Lander, A.D., Gokoffski, K.K., Wan, F., Nie, Q., and Calof, A.L. (2009) Cell Lineages and the logic of proliferative control. PLoS Biology 7(1): e1000015. doi:10.1371/journal.pbio.1000015. ** Reviewed in G.T. Reeves & S.E. Fraser (2009) “Biological Systems from an Engineer’s Point of View”, PLoS Biology Primer, PLoS Biol 7(1): e1000021. https://doi.org/10.1371/journal.pbio.1000021
Lo, W-C, Chou, C-S, Gokoffski, KK, Wan, FYM, Lander, AD, Calof, AL, and Nie, Q (2009) Feedback regulation in multistage cell lineages. Mathematical Biosciences and Engineering, 6(1): 59-82.
Hamilton, JA, Beites, CL, Gokoffski, KK, Hollenbeck PLW, Kawauchi, S, Santos R, Bonnin A, Wu HH, Kim J, & Calof, A.L. (2008) Negative regulation of endogenous stem cells in sensory neuroepithelia: implications for neurotherapeutics. Stem Cell Research and Therapeutics, Y. Shi, D. Clegg (Eds.) Springer, pp. 45-68.
Ogata, S., Kawauchi, S. Calof, A., and Cho, K.W.Y. (2007) Plastic embedding and sectioning of Xenopus laevis embryos. Journal of Visualized Experiments, http://www.jove.com/index/Details.stp?ID=188.
Kawauchi S., Shou, J., Santos R., Hebert J., McConnell S.K., Mason, I., and Calof, A.L. (2005) Fgf8 expression defines a morphogenetic center required for olfactory neurogenesis and nasal cavity development in the mouse. Development, 132: 5211-5223. ** Reviewed in Development (J. Bradbury, “Fgf8 noses into olfactory development”; Development 2005 132: 2303).
Kim, J., Wu, H.-H., Lander, A.D., Lyons, K.M., Matzuk, M. M., and Calof, A.L. (2005). GDF11 controls the timing of progenitor cell competence in developing retina. Science 308: 1927-1930. ** Reported/reviewed in Science (This Week in Science, “Calling New Neurons” Vol. 308, p.1838); the Orange County Register (June 24, 2005); the Santa Barbara News-Press (June 25, 2005); Obesity, Fitness, and Wellness Week (July 16, 2005), and online at: http://today.uci.edu/news/release_detail.asp?key=1344); http://www.blindness.org/research.asp?id=253; Sci. STKE, Vol. 2005, Issue 290, pp. tw236, 28 June 2005 [DOI: 10.1126/stke.2902005tw236]
Beites, C., Kawauchi, S., Crocker, C.E., and Calof, A.L. (2005) Identification and molecular regulation of neural stem cells in the olfactory epithelium. Experimental Cell Research 306: 309-316.
Kawauchi, S., Beites, C., Crocker, C., Wu, H.-H., Bonnin, A., Murray, R., and Calof, A.L. (2004) Molecular regulation of neurogenesis in the olfactory receptor neuron lineage. Developmental Neuroscience 26: 166-180.
Krantz, I.D., McCallum, J., DeScipio, C., Kaur, M., Gillis, L., Yaeger, D., Jukofsky, L., Wasserman, N., Bottani, A., Morris, C.A., Nowaczyk, N., Toriello, H., Bamshad, M.J., Carey, J.C., Rappaport, E., Kawauchi, S., Lander, A.D., Calof, A.L., Ki, H.-H., Devoto, M., and Jackson, L.G. (2004) Cornelia de Lange Syndrome is caused by mutations in NIPBL, the human homolog of the Drosophila Nipped-B gene. Nature Genetics 36: 631-635. ** Reviewed in “ ‘Nipped’ gene holds key to birth defect”, www.excellence-earlychildhood.ca/documents/Page9Vol4No2Oct05ANG.pdf
Wu, H. -H., Ivkovic, S., Murray, R. C., Jaramillo, S., Lyons, K. M., Johnson, J. E., and Calof, A. L. (2003). Autoregulation of neurogenesis by GDF11. Neuron 37: 197-207. ** Reviewed in News & Views in Nature Medicine (N.B. Hastings and E. Gould, “Neurons Inhibit Neurogenesis”, 2003, vol. 9, pp. 264-266) and Developmental Cell (L.W. Garner, J. Nove, and V Rosen, “Return of the Chalones”, 2003, vol. 4, pp. 149-151).
Murray, R.C., Navi, D., Fesenko, J., Lander, A.D., and Calof, A.L. (2003) Widespread defects in the developing mammalian olfactory system caused by loss of Mash1 function. The Journal of Neuroscience 23: 1769-1780.
Calof, A.L., Bonnin, A., Crocker, C., Kawauchi, S., Murray, R., Shou, J., and Wu, H.-H. (2002) Progenitor cells of the olfactory receptor neuron lineage. Microsc. Res. Tech. 58: 176-188.
Calof, A.L. (2000) Long odds. Current Biology 10: R539.
Shou, J., Murray, R. C., Rim, P.C., Kim, Y.C., and Calof, A.L. (2000) Opposing effects of bone morphogenetic proteins on neuron production and survival in the olfactory receptor neuron lineage. Development 127: 5403-5413.
Murray, R.C., Tapscott, S.J., Petersen, J.M, Calof, A.L., and McCormick, M.B. (2000). A fragment of the neurogenin1 gene confers regulated expression of a reporter gene in vitro and in vivo. Developmental Dynamics 218: 189-194.
Calof, A.L. (1999) Grant-writing amnesia. Current Biology 9: R869.
Calof, A.L., Mumm, J.S., Rim, P. and Shou, J. (1999) In vitro analysis of neuronal progenitor cells from mouse olfactory epithelium. In: The Neuron in Tissue Culture (L. Haynes, Ed.) Wiley, Chichester,pp. 23-44.
Murray, R.C. and Calof, A.L. (1999) Neuronal regeneration: Lessons from the olfactory system. Seminars in Cell & Developmental Biology 10: 421-431.
Shou, J., Rim, P.C., and Calof, A.L. (1999) BMPs inhibit neurogenesis by a mechanism involving degradation of a transcription factor. Nature Neuroscience 2: 339-345. ** Reviewed in News and Views by G. Fishell, 1999, “BMPs: Time to Murder and Create”, Nature Neuroscience 2, 301 - 303 (1999) doi:10.1038/7208.
Calof, A.L. (1998) Overcommitment. Current Biology 8: R107.
Calof, A.L., Rim, P.C, Askins, K.J., Mumm, J.S., Gordon, M.K., Iannuzzelli, P., and Shou, J. (1998) Factors regulating neurogenesis and programmed cell death in mouse olfactory epithelium. In: Olfaction and Taste XII (C. Greer and C. Murphy, eds.) New York, Annals of the New York Academy of Sciences 855, pp. 226-229.
Calof, A.L., Mumm, J.S., Rim, P.C, and Shou. J. (1998) The neuronal stem cell of the olfactory epithelium. J. Neurobiol. 36: 190-205
Calof, A.L., Holcomb, J.D., Mumm, J.S., Hagiwara, N., Tran, P., Smith, K.M., and Shelton, D.L. (1996) Factors affecting neuronal birth and death in mammalian olfactory epithelium. In: Growth Factors as Drugs for Neurological and Sensory Disorders (G.R. Bock and J.A. Goode, eds.) Wiley, Chichester (Ciba Foundation Symposium 196), pp. 188-210.
Mumm, J.S., Shou, J., and Calof, A.L. (1996) Colony-forming progenitors from mouse olfactory epithelium: Evidence for feedback regulation of neuron production. Proc. Natl. Acad. Sci. USA 93: 11167-11172.
Holcomb, J.D., Graham, S., and Calof, A.L. (1996) Neuronal homeostasis in mammalian olfactory epithelium: A review. Am. J. Rhinol. 10: 125-134.
Calof, A.L., Hagiwara, N., Holcomb, J.D., Mumm, J.S., and Shou, J. (1996) Neurogenesis and cell death in the olfactory epithelium. J. Neurobiol. 30: 67-81.
Calof, A.L., Guevara, J.G., and DeHamer, M.K. (1995) Mouse olfactory epithelium. In: Primary Neuronal Cell Culture: A Practical Approach. (J. Cohen and G. Wilken, eds.) Oxford, IRL Press, pp. 205-220.
Holcomb, J.D., Mumm, J.S. and Calof, A.L. (1995) Apoptosis in the neuronal lineage of the mammalian olfactory epithelium: Regulation in vivo and in vitro. Devel. Biol. 172: 307-323.
Gordon, M.K., Mumm, J.S., Davis, R.A., Holcomb, J.D. and Calof, A.L. (1995) Dynamics of MASH-1 expression in vitro and in vivo suggest a non-stem cell site of MASH-1 action in the olfactory receptor neuron lineage. Mol. Cell. Neurosci. 6: 363-379.
Calof, A.L. (1995) Intrinsic and extrinsic factors regulating vertebrate neurogenesis. Current Opinion in Neurobiology 5: 19-27.
Calof, A.L., Adusumalli, M., DeHamer, M., Guevara, J.L., Mumm, J.S., Whitehead, S., and Lander, A.D. (1994) Generation, differentiation, and maturation of olfactory receptor neurons in vitro. In: Olfaction and Taste XI (K. Kurihara, N. Suzuki, H. Ogawa, eds.) Tokyo, Springer-Verlag, pp. 36-40.
DeHamer, M., Guevara, J., Hannon, K., Olwin, B., and Calof, A.L. (1994) Genesis of olfactory receptor neurons: Regulation of progenitor cell divisions by fibroblast growth factors. Neuron 13: 1083-1097.
Calof, A.L., Campanero, M.R., Yurchenco, P.D., and Lander, A.D. (1994) Domain-specific activation of the neuronal migration and neurite outgrowth activities of laminin. Neuron, 13: 117-130.
Lander, A.D. and Calof, A.L. (1993) Extracellular matrix in the developing nervous system. In: Molecular Genetics of Nervous System Tumors. (A.J. Levine and H.H. Schmidek, Eds.) Wiley, New York, pp. 341-355.
Calof, A.L. and Guevara, J. L. (1993) Cell lines derived from retrovirus-mediated oncogene transduction into olfactory epithelium cultures. NeuroProtocols 3: 222-231.
Calof AL. (1993) Immortalizing neural cells -- Overview. NeuroProtocols 3:175.
Trevino, C., Calof, A.L., and Muneoka, K. (1992) Position specific growth regulation of 3T3 cells in vivo. Dev. Biol. 150: 72-81.
Calof, A.L. (1992) Sex, nose and genotype. Current Biology 2: 103-105.
Calof, A.L., Lander, A.D., and Chikaraishi, D.M. (1991) Regulation of neurogenesis and neuronal differentiation in primary and immortalized cells from mouse olfactory epithelium. In: Regeneration of Vertebrate Sensory Receptor Cells. Wiley, Chichester (Ciba Foundation Symposium 160), pp. 249-276.
Calof, A.L. and Lander, A.D. (1991) Relationship between neuronal migration and cell-substratum adhesion: laminin and merosin promote olfactory neuronal migration but are anti-adhesive. J. Cell Biol. 115: 779-794.
Calof, A.L. (1991) Immortalized neurons derived from tumors in transgenic mice. Trends in Neurosciences 14: 1-3.
Calof, A.L. and Chikaraishi, D.M. (1989) Analysis of neurogenesis in a mammalian neuroepithelium: Proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3: 115-127.
Calof, A.L. and Reichardt, L.F. (1985) Response of purified chick motoneurons to myotube conditioned medium: Laminin is essential for substratum-binding, neurite outgrowth-promoting activity. Neuroscience Letters 59: 183-189.
Calof, A.L. and Reichardt, L.F. (1984) Motoneurons purified by cell sorting respond to two distinct activities in myotube conditioned medium. Dev. Biol. 106: 194-210.
Lander, A.D. Tomaselli, K.J., Calof, A.L., and Reichardt, L.F. (1983) Studies on extracellular matrix components that promote neurite outgrowth. C.S.H. Symp. Quant. Biol. 48: 611-623.
Calof, A.L., Jones, R.B., and Roberts, W.J. (1981) Sympathetic modulation of mechanoreceptor sensitivity in frog skin. J. Physiol. 310: 481-499.
Society for Neuroscience
Society for Developmental Biology
American Society for Cell Biology
Association for Chemoreception Sciences
Genetics Society of America
Cellular and Molecular Biosciences
Interdepartmental Neuroscience Program
Mathematical and Computational Biology
Developmental Biology Center
Chao Comprehensive Cancer Center
Cancer Research Institute
UCI Center for Complex Biological Systems
UCI Center for Hearing Research
UCI Sue and Bill Gross Stem Cell Research Center