Alan L. Johnson

Alan L. Johnson

  • Walther H. Ott Professor in Avian Biology


  • Ph.D. Physiology, Cornell University, 1979
  • M.S. Zoology, University of Vermont, 1975
  • B.A. Zoology, University of Vermont, 1972

Professional Experience

  • Walther H. Ott Professor in Avian Biology, Department of Animal Science, The Pennsylvania State University, July 1, 2009-present
  • Professor of Physiology, Department of Biological Sciences, University of Notre Dame, 1993-2009
  • Visiting Scientist, Department of Animal Sciences/Molecular Biology Program, University of Missouri, Columbia, September 1991-August 1992 (12-month sabbatical leave)
  • Professor, Department of Animal Sciences, Rutgers University, 1990-1993
  • Associate Professor with tenure, Department of Animal Sciences, Rutgers University, 1984-1990
  • Director of the Graduate Program in Animal Sciences, Rutgers University, 1986-1993
  • Associate Chair for Graduate Teaching and Research, Department of Animal Sciences, Rutgers University, 1986-1993
  • Assistant Professor, Department of Animal Sciences, Rutgers University, 1981-1984
  • Visiting Scientist, INRA, Station de Recherches Avicoles, Nouzilly, France, June-July 1980
  • Postdoctoral Research Associate, Cornell University, 1978-1981

Current Teaching

Undergraduate:  The Vertebrates (a lecture course within the Department of Wildlife and Fisheries; WFS300, 2 credits), and co-teach The Vertebrates Laboratory (WFS 301, 2 credits). Considers the evolution, taxonomy, anatomical/physiological adaptations and natural history of the vertebrate species.

Graduate: Co-teach Scientific Scholarship (AN SC 502, 2 credits). Consideration of scientific ethics (fulfills 'Scholarship and Research Integrity [SARI] Program requirement for Penn State University graduate students), the scientific method and thinking relative to scholarship, grantsmanship, and the mechanism of grantsmanship.

Program Objectives

Implications for the research in our laboratory pertain to both improving women's reproductive health, together with the broader objective of understanding patterns of ovarian function and follicle development among vertebrates whose reproductive strategy consists of producing a limited number of offspring combined with considerable maternal investment (e.g., mammals, birds and a few reptiles). Applications include the potential for enhancing the reproductive potential of threatened/endangered plus domesticated avian species, particularly broiler breeders in which an aberrant regulation of the follicular hierarchy results in suboptimal egg production.

Ovarian Follicle Selection

A major focus is to define the endocrine, cellular and molecular mechanisms that accomplish follicle selection, a process as yet undefined in any vertebrate. The selection of preovulatory follicles represents an event by which a species-specific number of ovarian follicles progresses from an undifferentiated to differentiated state in preparation for ovulation. This process is critical for maintaining normal reproductive cycles and is dependent upon a balance between the maintenance of follicle viability and the loss of excessive or nonviable follicles via follicle atresia. Notably, excessive atresia can ultimately result in infertility and/or early reproductive senescence (e.g., menopause). The domestic hen represents a unique and important animal model system for such studies due to the ability to reliably identify a small cohort of prehierarchal follicles from which a single follicle per day is recruited into the preovulatory hierarchy.

The working hypothesis of our ongoing studies is that follicle selection and final differentiation prior to ovulation results from the removal of inhibitory cell signaling within the granulosa cell layer. To date, the nature of inhibition has focused on MAPK/Erk and protein kinase C (PKC) cell signaling maintained by epidermal growth factor ligands (EGFL) produced in an autocrine and paracrine fashion. The alleviation from this inhibitory signaling within the selected follicle subsequently enables FSH-induced LH receptor (LHR) induction and the initiation of steroid production. Of particular note is the recent finding that following follicle selection, MAPK/Erk and PKC signaling transitions to become obligatory for the expression and optimal activity of steroidogenic acute regulatory (STAR) protein and maximal steroidogenesis required for ovulation.

Significantly, the selective loss of ovarian follicles by atresia occurs via apoptosis and this process is first evident within the granulosa cell layer. We have established that granulosa cells from atresia-susceptible prehierarchal follicles are highly susceptible to undergoing apoptosis, in vitro. By contrast, following selection for final differentiation preceding ovulation, preovulatory follicles are not normally subject to atresia, and cultured granulosa cells from such follicles are known to be highly resistant to apoptosis. Such studies are conducted using transfection to over-express single or multiple gene products in cultured cells as well as by the targeted decrease in expression following transfection with antisense constructs. For additional information and related publications pertaining to ovarian follicle growth, development and atresia mediated via apoptosis visit our web site at: AVIANOVA Web Site. On the other hand, a decrease or absence of normal apoptotic cell death can contribute to tumor formation. Accordingly, a second and related focus utilizes human granulosa tumor cell lines to assess the role of cell survival proteins and cell death pathways in tumor formation and resistance to chemotherapeutics.


Selected Publications

For a more complete listing: Johnson Publications

Poole, D.H., Ocón-Grove, O.M., Johnson, A.L. (2016) Anti-Müllerian Hormone Receptor Type II Expression and Anti-Müllerian Hormone Activity in Bovine Granulosa Cells. Theriogenology, In press. DOI:

Kim, D., Lee, J. and Johnson, A.L. (2016) Vascular endothelial growth factor and angiopoietins during hen ovarian follicle development. Gen. Comp. Endocrinol. 232: 25-31.

Kim, D. and Johnson, A.L. (2016) Vasoactive Intestinal Peptide Promotes Differentiation and Clock Gene Expression in Granulosa Cells from Prehierarchal Follicles. Mol. Reprod. Develop. 83: 455-463. doi: 10.1002/mrd.22641

Johnson, A.L. and Lee, J. (2015). Granulosa cell responsiveness to follicle stimulating hormone during early growth of hen ovarian follicles. Poultry Science 95: 108-114.

Johnson, A.L. (2014) The avian ovary and follicle development – some comparative and practical insights. Turkish Journal of Veterinary and Animal Sciences 38: 660-669. Invited Review. doi: 10.3906/vet-1405-6-A.

Johnson, A.L. (2014) Ovarian follicle selection, and granulosa cell differentiation. Poultry Science 94: 781-785.

Kim D, Ocón-Grove O, Johnson AL. (2013) Bone Morphogenetic Protein 4 (BMP4) Supports the Initial Differentiation of Hen (Gallus gallus) Granulosa Cells. Biol Reprod. 2013 88:161, 1-7.

Ocón-Grove, O.M., Poole, D.H. and Johnson, A.L. (2012) Bone morphogenetic protein 6 promotes FSH receptor and anti-Müllerian Hormone mRNA expression in granulosa cells from hen prehierarchal follicles. Reproduction 143:825-833.

Woods, D.C., White, Y.A.R., Dau, C. and Johnson, A.L. (2011) TLR4 activates NFB in human ovarian granulosa tumor cells. Biochem. Biophys. Res Comm. 409: 675-680.

Haugen, M.J. and Johnson, A.L. 2010. Bone morphogenetic protein 2 inhibits FSH responsiveness in hen granulosa cells. Reproduction 140:1-9.

Johnson, A.L. and Woods, D.C. 2009. Dynamics of avian follicle development: Cellular mechanisms of granulosa cell development. Gen. Comp. Endocrinol. 163:12-17.

Johnson, A.L., Haugen, M.J., Woods, D.C. 2008. Role for inhibitor of differentiation/DNA binding (Id) proteins in granulosa cell differentiation. Endocrinology 149:3187-3195.

Woods, D.C., Alvarez, C., Johnson, A.L. 2008. Cisplatin-mediated sensitivity to TRAIL-induced cell death in human granulosa tumor cells. Gynecol. Oncology 108:632-640.

Woods, D.C., Liu, H.-K., Nishi, Y., Yanase, T., Johnson, A.L. 2007. Inhibition of proteosome activity sensitizes human granulosa tumor cells to TRAIL-induced cell death. Cancer Letters 260:20-27.

Woods, D.C. and Johnson, A.L. 2006. Phosphatase activation by EGF family ligands regulates Erk signaling in undifferentiated hen granulosa cells. Endocrinology 147:4931-4940.

Woods D.C. and Johnson, A.L. 2005. Regulation of follicle-stimulating hormone receptor mRNA in hen granulosa cells relative to follicle selection. Biol. Reprod. 72:643-650.

Recent Book Chapters

Johnson, A.L. (1999) Reproduction in the female. In: Sturkie's Avian Physiology, 5th Ed., G.C. Whittow, Ed., New York: Academic Press, Chapter 22, pp. 569-596.
Johnson, A.L. (1999) Ovarian cycles and follicle development in birds. In: Encyclopedia of Reproduction, E. Knobil and J.D. Neill, Eds., New York:  Academic Press, Vol.3, pp. 564-574. 
Tilly, J.L. and A.L. Johnson (1999) Chemotherapy and apoptosis in the ovary: Cancer treatment comes with a price. In: Apoptosis and Cancer Chemotherapy.  J.A. Hickman and C. Dive, Eds.,  Humana Press, Inc.,  pp. 257-273.
Johnson, A.L. and D.C. Woods (2007) Chapter 6. Ovarian dynamics and follicle development. In: Reproductive Biology and Phylogeny of Aves, B.G.M. Jamieson, Ed., Science Publishers, Inc., pp. 243-277.
Johnson, A.L., Woods, D.C. (2009) Granulosa Cell Tumors. In: Encyclopedia of Cancer, second edition, M. Schwab, Ed. Springer. ISBN: 978-3-540-47649-8.
Johnson, A.L. (2010) Chapter 3: Hormones and Ovarian Structure and Function in Birds. In: Hormones and Reproduction of Vertebrates, Volume 4 – Birds. D.O. Norris and K.H. Lopez, Eds.  Academic Press, pp. 71-90.
Johnson, A.L. (2014) Reproduction in the female. In: Sturkie's Avian Physiology, 6th Ed., C.G. Scanes, Ed., New York: Elsevier, Chapter 28, pp.635-665.

Awards and Honors

  • Zoetis Fundamental Science Award, Poultry Science Association, 2015

  • Recipient of the Shilts-Leonard Teaching Award for the College of Science, University of Notre Dame, 2004
  • Recipient of the New Jersey Agricultural Experiment Station/Cook College, Rutgers University Research Excellence Award. Awarded for sustained research excellence during the previous five years, 1992

Previous Teaching

Undergraduate Teaching

  • Comparative Integrative Physiology (BIOS 30421, 4 credit lecture)
  • Comparative Integrative Physiology Laboratory (BIOS 31421L, 1 credit laboratory) 
  • Human Reproduction and Society (BIOS 109; 3 credit lecture); Fall Semester, 1995-2001
  • Ornithology field-course (BIOS 569), Practicum in Field Environmental Biology, UNDERC
  • Vertebrate Biology (BIOS 30404; 3 credit lecture/laboratory)
  • Serve as Independent Research Advisor for undergraduates during the academic year and/or for summer Fellowship programs (Howard Hughes, NSF/REU/SROP)

Graduate Teaching

  • Topics in Physiology: Reproduction, BIOS 575
  • Graduate Physiology Seminar, BIOS 580

Service to the Profession

  • Editorial Advisory Board, Animal Reproduction Science, July 2010 to present
  • Editorial Board, Poultry Science, 1982-1988, 1992-1995; Section Editor for Physiology, Endocrinology and Reproduciton, 2011 to present
  • Editorial Board, Journal of Animal Sciences, 1988-1991
  • Editorial Board, Domestic Animal Endocrinology, 1990-1993
  • Editorial Board, Journal of Endocrinology, 2008 to 2012
  • Board of Reviewing Editors, Biology of Reproduction, 2009 to 2012
  • Program Chair, Poultry Science Association Annual Meeting, 1989, University of Wisconsin
  • Member of USDA NRI Competitive Grants Program Review Panel, Reproductive Biology Section, Washington, D.C., 1989, 1990, 1993, 1994, 2003, 2004, 2006
  • USDA CSRS Review of University of Nebraska Department of Animal Science, 1993
  • NIH Biochemical Endocrinology Study Section, Bethesda, MD, June 2001
  • Program Chair, Society for the Study of Reproduction (SSR) Annual Meeting, Quebec City, Canada, 2005
  • NIH Cellular and Molecular Integrative Reproduction Study Section, Bethesda, MD, October, 2005
  • Society for the Study or Reproduction (SSR) representative to the Federation of American Societies for Experimental Biology (FASEB) Publications and Communication Committee. 2005-2013
  • NSF Integrative Organismal Systems Review Panel, Washington, DC, October 2009
  • Society for the Study of Reproduction (SSR), Publications Committee member, 2008 to 2012; Publications Committee Chair, 2012-2013