Skip to main content
SpringerLink
Log in

Cell Signaling Pathways in Vertebrate Lens Regeneration

  • Chapter
  • First Online:
Book cover New Perspectives in Regeneration

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 367))

Abstract

Certain vertebrates are capable of regenerating parts of the eye, including the lens. Depending on the species, two principal forms of in vivo lens regeneration have been described wherein the new lens arises from either the pigmented epithelium of the dorsal iris or the cornea epithelium. These forms of lens regeneration are triggered by retinal factors present in the eye. Studies have begun to illuminate the nature of the signals that support lens regeneration. This review describes evidence for the involvement of specific signaling pathways in lens regeneration, including the FGF, retinoic acid, TGF-beta, Wnt, and Hedgehog pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

BMP:

Bone morphogenetic protein

cDNA:

Complementary DNA

EGF:

Epidermal growth factor

EGFR:

Epidermal growth factor receptor

EST:

Expressed sequence tag

HH:

Hedgehog

FGF:

Fibroblast growth factor

FGFR:

Fibroblast growth factor receptor

IGF:

Insulin like growth factor

mRNA:

Messenger RNA

PECs:

Pigmented epithelial cells

PCP:

Planar cell polarity

RA:

Retinoic acid

RAREs:

Retinoic acid response elements

TGFβ:

Transforming growth factor-beta

VEGF:

Vascular endothelial growth factor

References

  • Allen BL, Tenzen T, McMahon AP (2007) The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev 21:1244–1257

    Article  PubMed  CAS  Google Scholar 

  • Ang SJ, Stump RJ, Lovicu FJ, McAvoy JW (2004) Spatial and temporal expression of Wnt and Dickkopf genes during murine lens development. Gene Expr Patterns 4:289–295

    Article  PubMed  CAS  Google Scholar 

  • Arresta E, Bernardini S, Gargioli C, Filoni S, Cannata SM (2005) Lens-forming competence in the epidermis of Xenopus laevis during development. J Exp Zool 303A:1–12

    Article  Google Scholar 

  • Atkinson DL, Stevenson TJ, Park EJ, Riedy MD, Milash B, Odelberg SJ (2006) Cellular electroporation induces dedifferentiation in intact newt limbs. Dev. Biol. 299:257–271

    Article  PubMed  CAS  Google Scholar 

  • Belecky-Adams TL, Adler R, Beebe DC (2002) Bone morphogenetic protein signaling and the initiation of lens fiber cell differentiation. Development 129:3795–3802

    PubMed  CAS  Google Scholar 

  • Blobe G, Liu X, Fang SJ, How T, Lodish HF (2001) A novel mechanism for regulating transforming growth factor β (TGF-β) signaling. Functional modulation of type III TGF-b receptor expression through interaction with the PDZ domain protein. GIPC. J. Biol. Chem 276:39608–39617

    Article  CAS  Google Scholar 

  • Bosco L, Venturini G, Willems D (1994) First evidence of lens-transdifferentiation of larval Xenopus laevis induced by brain-derived acidic FGF. Rendiconti Lincei 5:261–268

    Article  Google Scholar 

  • Bosco L, Venturini G, Willems D (1997) In vitro lens transdifferentiation of Xenopus laevis outer cornea induced by Fibroblast Growth Factor (FGF). Development 124:421–428

    PubMed  CAS  Google Scholar 

  • Chamberlain C, McAvoy J (1997) Fibre differentiation and polarity in the mammalian lens: a key role for FGF. Progress in Retinal and Eye Research 16:443–478

    Article  CAS  Google Scholar 

  • Chen Y, Stump RJ, Lovicu FJ, McAvoy JW (2004) Expression of frizzleds and secreted frizzled-related proteins (Sfrps) during mammalian lens development. Int J Dev Biol 48:867–877

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Stump RJ, Lovicu FJ, McAvoy JW (2006) A role for Wnt/planar cell polarity signaling during lens fiber cell differentiation? Semin Cell Dev Biol 17:712–725

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Stump RJ, Lovicu FJ, Shimono A, McAvoy JW (2008) Wnt signaling is required for organization of the lens fiber cell cytoskeleton and development of lens three-dimensional architechture. Dev Biol 324:161–176

    Article  PubMed  CAS  Google Scholar 

  • Chuang PT, McMahon AP (1999) Vertebrate hedgehog signaling modulated by induction of a hedgehog-binding protein. Nature 397(6720):617–621

    Article  PubMed  CAS  Google Scholar 

  • Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127:469–480

    Article  PubMed  CAS  Google Scholar 

  • Cousins SW, McCabe MM, Danielpour D, Streilein W (1991) Identification of transforming growth factor-beta as an immunosuppressive factor in aqueous humor. Invest Ophthalmol Vis Sci 32:2201–2211

    PubMed  CAS  Google Scholar 

  • Cvekl A, Wang WL (2009) Retinoic acid signaling in mammalian eye development. Exp Eye Res 89:280–291

    Article  PubMed  CAS  Google Scholar 

  • Dailey L, Ambrosetti D, Mansukhani A, Basilico C (2005) Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev 16:233–247

    Article  PubMed  CAS  Google Scholar 

  • Day RC, Beck CW (2011) Transdifferentiation from cornea to lens in Xenopus laevis depends on BMP signaling and involves upregulation of Wnt signaling. BMC Dev Biol 11:54

    Article  PubMed  CAS  Google Scholar 

  • De A (2011) Wnt/Ca2 + signaling pathway: a brief overview. Acta Biochim Biophys Sin 43:745–756

    Article  PubMed  CAS  Google Scholar 

  • Del Rio-Tsonis K, Jung JC, Chiu I-M, Tsonis PA (1997) Conservation of fibroblast growth factor function in lens regeneration. Proc Natl Acad Sci 94:13701–13706

    Article  PubMed  Google Scholar 

  • Del Rio-Tsonis K, Trombley MT, McMahon G, Tsonis PA (1998) Regulation of lens regeneration by fibroblast growth factor receptor 1. Dev Dyn 213:140–146

    Article  PubMed  CAS  Google Scholar 

  • DeRobertis EM, Kuroda H (2004) Dorsal–ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20:285–308

    Article  CAS  Google Scholar 

  • Donner A, Lachke S, Maas R (2006) Lens induction in vertebrates: variations on a conserved theme of signaling events. Semin Cell Dev Biol 17:676–685

    Article  PubMed  CAS  Google Scholar 

  • Dorey K, Amaya E (2010) FGF signaling: diverse roles during early vertebrate embryogenesis. Development 137:3731–3742

    Article  PubMed  CAS  Google Scholar 

  • Ekker SC, Ungar AR, Greenstein P, von Kessler DP, Porter JA, Moon RT, Beachy PA (1995) Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr Biol 5(8):944–955

    Article  PubMed  CAS  Google Scholar 

  • Enwright JF, Grainger RM (2000) Altered retinoid signaling in the heads of small eye mouse embryos. Dev. Biol 221:10–22

    Article  PubMed  CAS  Google Scholar 

  • Faber SC, Robinson ML, Makarenkova HP, Lang RA (2002) Bmp signaling is required for development of primary lens fiber cells. Development 129:3727–3737

    PubMed  CAS  Google Scholar 

  • Filoni S, Bernardini S, Cannata SM (2006) Experimental analysis of lens-forming capacity in Xenopus borealis larvae. J Exp Zool 305:538–550

    Google Scholar 

  • Freeman G (1963) Lens regeneration from the cornea in Xenopus laevis. J Exp Zool 154:39–66

    Article  PubMed  CAS  Google Scholar 

  • Fuhrmann S (2008) Wnt signaling in eye organogenesis. Organogenesis 4:60–67

    Article  PubMed  Google Scholar 

  • Fukui L, Henry JJ (2011) FGF signaling is required for lens regeneration in Xenopus laevis. Biol Bull 221:137–145

    PubMed  CAS  Google Scholar 

  • Furuta Y, Hogan BLM (1998) BMP4 is essential for lens induction in the mouse embryo. Genes Dev 12:3764–3775

    Article  PubMed  CAS  Google Scholar 

  • Gao C, Chen YG (2010) Dishevelled: the hub of Wnt signaling. Cell Signal 22:717–727

    Article  PubMed  CAS  Google Scholar 

  • Garcia CM, Huang J, Madakashira BP, Liu Y, Rajagopal R, Dattilo L, Robinson ML, Beebe DC (2011) The function of FGF signaling in the lens placode. Dev Biol 351:176–185

    Article  PubMed  CAS  Google Scholar 

  • Goodrich LV, Johnson RL, Milenkovic L, McMahon JA, Scott MP (1996) Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev 10:301–312

    Article  PubMed  CAS  Google Scholar 

  • Gopal-Srivastava R, Cvekl A, Piatigorsky J (1998) Involvement of retinoic acid/retinoid receptors in the regulation of murine alphaB-crystallin/small heat shock protein gene expression in the lens. J Biol Chem 273:17954–17961

    Article  PubMed  CAS  Google Scholar 

  • Granstein RD, Staszewski R, Knisely TL, Zeira E, Nazareno R, Latina M, Albert DM (1990) Aqueous humor contains transforming growth factor- beta and a small (<3500 daltons) inhibitor of thymocyte proliferation. J Immunol 144:3021–3027

    PubMed  CAS  Google Scholar 

  • Grogg MW, Call MK, Okamoto M, Vergara MN, Tsonis PA (2005) BMP inhibition-driven regulation of six-3 underlies induction of newt lens regeneration. Nature 438:858–862

    Article  PubMed  CAS  Google Scholar 

  • Gunhaga L (2011) The lens: a classical model of embryonic induction providing new insights into cell determination in early development. Philos Trans R Soc Lond B Biol Sci 366:1193–1203

    Article  PubMed  Google Scholar 

  • Hayashi T, Mizuno N, Owaribe K, Kuroiwa A, Okamoto M (2002) Regulated lens regeneration from isolated pigmented epithelial cells of newt iris in culture in response to FGF2/4. Differentiation 70:101–108

    Article  PubMed  CAS  Google Scholar 

  • Hayashi T, Mizuno N, Ueda Y, Okamoto M, Kondoh H (2004) FGF2 triggers iris-derived lens regeneration in newt eye. Mech Dev 121:519–526

    Article  PubMed  CAS  Google Scholar 

  • Hayashi T, Mizuno N, Takada R, Takada S, Kondoh H (2006) Determinative role of Wnt signals in dorsal iris-derived lens regeneration in newt eye. Mech Dev 123:793–800

    Article  PubMed  CAS  Google Scholar 

  • Henry JJ (2003) Cell and molecular biology of lens regeneration. Int Rev Cytol Surv Cell Biol 228:195–264

    CAS  Google Scholar 

  • Henry JJ, Elkins ME (2001) Cornea lens transdifferentiation in Xenopus tropicalis. Dev Genes Evol 211:377–387

    Article  PubMed  CAS  Google Scholar 

  • Henry JJ, Tsonis PA (2010) Molecular and cellular aspects of amphibian lens regeneration. Prog Retinal Eye Res 29:543–555

    Article  CAS  Google Scholar 

  • Henry JJ, Carinato ME, Schaefer JJ, Wolfe AD, Walter BE, Perry KJ, Elbl TN (2002) Characterizing gene expression during lens formation in Xenopus laevis: evaluating the model for embryonic lens induction. Dev Dyn 224:168–185

    Article  PubMed  CAS  Google Scholar 

  • Henry JJ, Wever JA, Veragara MN, Fukui L (2008) Ch. 6. Xenopus, an ideal vertebrate system for studies of eye development and regeneration. In: Tsonis, PA (ed) Animal models for eye research. Academic Press, San Diego, CA

    Google Scholar 

  • Hyatt GA, Schmitt EA, Marsh-Armstrong N, McCaffery P, Drager UC, Dowling JE (1996) Retinoic acid establishes ventral retinal characteristics. Development 122:195–204

    PubMed  CAS  Google Scholar 

  • Ikeda Y (1936a) Neue versuche zur analyse de Wolffschen linsregeneration. Arb Anat Inst Kais Jpn Univ Sendai 18:1–16

    Google Scholar 

  • Ikeda Y (1936b) Beiträge zur frage der fähigkeit zur linsenregeneration bei einer Art von Hynobius (Hynobius unnangso Tago). Arb Anat Inst Kais Jpn Univ Sendai 18:17–50

    Google Scholar 

  • Ikeda Y (1939) Zur frage der lensenpotenz der hornhaut in spätembryonalen und larvvalen stadien bei ener Art von Hynobius (Hynobius unnangso Tago). Arb Anat Inst Kais Jpn Univ Sendai 22:27–52

    Google Scholar 

  • Ingham PW, McMahon AP (2001) Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15:3059–3087

    Article  PubMed  CAS  Google Scholar 

  • Ingham PW, Nakano Y, Seger C (2011) Mechanisms and functions of hedgehog signaling across the metazoa. Nat Rev Genet 12(6):393–406

    Article  PubMed  CAS  Google Scholar 

  • Itoh N (2007) The Fgf families in humans, mice, and zebrafish: their evolutional processes and roles in development, metabolism, and disease. Biol Pharm Bull 30:1819–1825

    Article  PubMed  CAS  Google Scholar 

  • Itoh N, Ornitz DM (2011) Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem 149:121–130

    Article  PubMed  CAS  Google Scholar 

  • Jampel HD, Roche N, Stark WJ, Roberts AB (1990) Transforming growth factor-beta in human aqueous humor. Curr Eye Res 9:963–969

    Article  PubMed  CAS  Google Scholar 

  • Johnson RL, Rothman AL, Xie J, Goodrich LV, Bare JW, Bonifas JM, Quinn AG, Myers RM, Cox DR, Epstein EH Jr, Scott MP (1996) Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 272:1668–1671

    Article  PubMed  CAS  Google Scholar 

  • Kastner P, Grondona JM, Mark M, Gansmuller A, LeMeur M, Decimo D, Vonesch JL, Dollé P, Chambon P (1994) Genetic analysis of RXR alpha developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 78(6):987–1003

    Article  PubMed  CAS  Google Scholar 

  • Kreslova J, Machon O, Ruzickova J, Lachova J, Wawrousek EF, Kemler R, Krauss S, Piatigorsky J, Kozmik Z (2007) Abnormal lens morphogenesis and ectopic lens formation in the absence of beta-catenin function. Genesis 45:157–168

    Article  PubMed  CAS  Google Scholar 

  • Kurosaka D, Nagamoto T (1994) Inhibitory effect of TGF-beta 2 in human aqueous humor on bovine lens epithelial cell proliferation. Invest Ophthalmol Vis Sci 35:3408–3412

    PubMed  CAS  Google Scholar 

  • Liu J, Hales AM, Chamberlain CG, McAvoy JW (1994) Induction of cataract-like changes in rat lens epithelial explants by transforming growth factor beta. Invest Ophthalmol Vis Sci 35:388–401

    PubMed  CAS  Google Scholar 

  • Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810

    Article  PubMed  CAS  Google Scholar 

  • Lovicu FJ, Overbeek PA (1998) Overlapping effects of different members of the FGF family on lens fiber differentiation in transgenic mice. Development (Cambridge, England) 125:3365–3377

    Google Scholar 

  • Luo G, Hofmann C, Bronckers AL, Sohocki M, Bradley A, Karsenty G (1995) BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev 9:2808–2820

    Article  PubMed  CAS  Google Scholar 

  • Macdonald R, Barth KA, Xu Q, Holder N, Mikkola I, Wilson SW (1995) Midline signaling is required for Pax gene regulation and patterning of the eyes. Development 121(10):3267–3278

    PubMed  CAS  Google Scholar 

  • MacDonald BT, Tamai K, He X (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9–26

    Article  PubMed  CAS  Google Scholar 

  • Machon O, Kreslova J, Ruzickova J, Vacik T, Klimova L, Fujimura N, Lachova J, Kozmik Z (2010) Lens morphogenesis is dependent on Pax6-mediated inhibition of the canonical Wnt/beta-catenin signaling in the lens surface ectoderm. Genesis 48:86–95

    PubMed  CAS  Google Scholar 

  • Makarev E, Call M, Crogg M, Atkinson DL, Milash B, Odelberg SJ, Tsonis PA (2007) Gene expression signatures in the newt irises during lens regeneration. FEBS Lett 581:1865–1870

    Article  PubMed  CAS  Google Scholar 

  • Maki N, Martinson J, Nishimura O, Tarui H, Meller J, Tsonis PA, Agata K (2010) Expression profiles during dedifferentiation in newt lens regeneration revealed by expressed sequence tags. Mol Vis 16:72–87

    PubMed  CAS  Google Scholar 

  • Malloch EM, Perry KJ, Fukui L, Johnson V, Wever J, Beck CW, King MW, Henry JJ (2009) Gene expression profiles of lens regeneration and development in Xenopus laevis. Dev Dyn 238:2340–2356

    Article  PubMed  CAS  Google Scholar 

  • Martinelli DC, Fan CM (2007) Gas1 extends the range of Hedgehog action by facilitating its signaling. Genes Dev 21:1231–1243

    Article  PubMed  CAS  Google Scholar 

  • Mason I (2007) Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat Rev Neurosci 8:583–596

    Article  PubMed  CAS  Google Scholar 

  • Massagué J, Seoane J, Wotton D (2005) Smad transcription factors. Genes Dev 19:2783–2810

    Article  PubMed  Google Scholar 

  • McDevitt D, Brahma SK, Courtois Y, Jeanny J-C (1997) Fibroblast growth factor receptors and regeneration of the eye lens. Dev Dyn 208:220–226

    Article  PubMed  CAS  Google Scholar 

  • Molotkov A, Deltour L, Foglio MH, Cuenca AE, Duester G (2002a) Distinct retinoid metabolic functions for alcohol dehydrogenase genes Adh1 and Adh4 in protection against vitamin A toxicity or deficiency revealed in double null mutant mice. J Biol Chem 277:13804–13811

    Article  PubMed  CAS  Google Scholar 

  • Molotkov A, Fan X, Duester G (2002b) Excessive vitamin A toxicity in mice genetically deficient in either alcohol dehydrogenase Adh1 or Adh3. Eur J Biochem 269:2607–2612

    Article  PubMed  CAS  Google Scholar 

  • Molotkov A, Molotkova N, Duester G (2006) Retinoic acid guides eye morphogenetic movements via paracrine signaling but is unnecessary for retinal dorsoventral patterning. Development 133:1901–1910

    Article  PubMed  CAS  Google Scholar 

  • Moustakas A, Heldin CH (2009) The regulation of TGFbeta signal transduction. Development 136:3699–3714

    Article  PubMed  CAS  Google Scholar 

  • Niederreither K, Dolle P (2008) Retinoic acid in development: toward an integrated view. Nat Rev Genet 9:541–553

    Article  PubMed  CAS  Google Scholar 

  • Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271:15292–15297

    Article  PubMed  CAS  Google Scholar 

  • Perron M, Boy S, Amato MA, Viczian A, Koebernick K, Pieler T, Harris WA (2003) A novel function for hedgehog signaling in retinal pigment epithelium differentiation. Development 130:1565–1577

    Article  PubMed  CAS  Google Scholar 

  • Perry KJ, Henry JJ (2012) Expression of pluripotency factors in the cornea epithelium of the frog Xenopus: evidence for the presence of epithelial stem cells (Submitted for Publication***)

    Google Scholar 

  • Robinson ML (2006) An essential role for FGF receptor signaling in lens development. Semin Cell Dev Biol 17:726–740

    Article  PubMed  CAS  Google Scholar 

  • Robinson ML, Ohtaka-Maruyama C, Chan CC, Jamieson S, Dickson C, Overbeek PA, Chepelinsky AB (1998) Disregulation of ocular morphogenesis by lens-specific expression of FGF-3/int-2 in transgenic mice. Dev Biol 198:13–31

    Article  PubMed  CAS  Google Scholar 

  • Roddy M, Tsonis PA (2008) The newt as a model for eye regeneration. In: Tsonis PA, (ed). Animal models for eye research. Academic Press, San Diego, CA

    Google Scholar 

  • Roddy M, Fox TP, McFadden JP, Nakamura K, Del Rio-Tsonis K, Tsonis PA (2008) A comparative proteomic analysis during urodele lens regeneration. Biochem Biophys Res Commun 377:275–279

    Article  PubMed  CAS  Google Scholar 

  • Saika S, Okada Y, Miyamoto T, Ohnishi Y, Ooshima A, McAvoy JW (2001) Smad translocation and growth suppression in lens epithelial cells by endogenous TGFbeta2 during wound repair. Exp Eye Res 72:679–686

    Article  PubMed  CAS  Google Scholar 

  • Saika S, Kono-Saika S, Ohnishi Y, Sato M, Muragaki Y, Ooshima A, Flanders KC, Yoo J, Anzano M, Liu C, Kao WW, Roberts AB (2004) Smad3 signaling is required for epithelial-mesenchymal transition of lens epithelium after injury. Am J Pathol 164:651–663

    Article  PubMed  CAS  Google Scholar 

  • Santander C, Brandan E (2006) Betaglycan induces TGF-beta signaling in a ligand-independent manner, through activation of the p38 pathway. Cell Signal 18:1482–1491

    Article  PubMed  CAS  Google Scholar 

  • Sasaki H, Nishizaki Y, Hui C, Nakafuku M. Kondoh H (1999) Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 126:3915–3924

    Google Scholar 

  • Schulz MW, Chamberlain CG, de Iongh RU, McAvoy JW (1993) Acidic and basic FGF in ocular media and lens: implications for lens polarity and growth patterns. Development 118:117–126

    PubMed  CAS  Google Scholar 

  • Smith AN, Miller LA, Song N, Taketo MM, Lang RA (2005) The duality of beta-catenin function: a requirement in lens morphogenesis and signaling suppression of lens fate in periocular ectoderm. Dev Biol 285:477–489

    Article  PubMed  CAS  Google Scholar 

  • Stolen CM, Jackson MW, Griep AE (1997) Overexpression of FGF-2 modulates fiber cell differentiation and survival in the mouse lens. Development 124:4009–4017

    PubMed  CAS  Google Scholar 

  • Stone DM, Hynes M, Armanini M, Swanson TA, Gu Q, Johnson RL, Scott MP, Pennica D, Goddard A, Phillips H, Noll M, Hooper JE, de Sauvage F, Rosenthal A (1996) The tumor-suppressor gene patched encodes a candidate receptor for sonic hedgehog. Nature 384(6605):129–134

    Article  PubMed  CAS  Google Scholar 

  • Stump RJ, Ang S, Chen Y, von Bahr T, Lovicu FJ, Pinson K, de Iongh RU, Yamaguchi TP, Sassoon DA, McAvoy JW (2003) A role for Wnt/beta-catenin signaling in lens epithelial differentiation. Dev Biol 259:48–61

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama Y, Stump RJ, Nguyen A, Wen L, Chen Y, Wang Y, Murdoch JN, Lovicu FJ, McAvoy JW (2010) Secreted frizzled-related protein disrupts PCP in eye lens fiber cells that have polarized primary cilia. Dev Biol 338:193–201

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama Y, Lovicu FJ, McAvoy JW (2011) Planar cell polarity in the mammalian eye lens. Organogenesis 7:191–201

    Article  PubMed  Google Scholar 

  • Tsonis PA, Trombley MT, Rowland T, Chandraratna RAS, Del Rio-Tsonis K (2000) Role of retinoic acid in lens regeneration. Dev Dyn 219:588–593

    Article  PubMed  CAS  Google Scholar 

  • Tsonis PA, Tsavaris M, Call MK, Chandraratna RAS, Del Rio-Tsonis K (2002) Expression and role of retinoic acid receptor alpha in lens regeneration. Dev Growth Differ 44:391–394

    Article  PubMed  CAS  Google Scholar 

  • Tsonis PA, Vergara MN, Spence JR, Madhavan M, Kramer EL, Call MK, Santiago WG, Vallance JE, Robbins DJ, Rio-Tsonis KD (2004) A novel role of the hedgehog pathway in lens regeneration. Dev Biol 267:450–461

    Article  PubMed  CAS  Google Scholar 

  • van den Heuvel M, Ingham PW (1996) Smoothened encodes a receptor-like serpentine protein required for hedgehog signaling. Nature 382:547–551

    Article  PubMed  Google Scholar 

  • Wagner E, McCaffery P, Dräger UC (2000) Retinoic acid in the formation of the dorsoventral retina and its central projections. Dev Biol 222(2):460–470

    Article  PubMed  CAS  Google Scholar 

  • Wawersik S, Purcell P, Rauchman M, Dudley AT, Robertson EJ, Maas R (1999) BMP7 acts in murine lens placode development. Dev. Biol 207:176–188

    Article  PubMed  CAS  Google Scholar 

  • Yang EV, Wang L, Tassava RA (2005) Effects of exogenous FGF-1 treatment on regeneration of the lens and the neural retina in the Newt, Notophthalmus viridescens. J Exp Zool 303A:837–844

    Article  CAS  Google Scholar 

  • Yang C, Yang Y, Brennan L, Bouhassira EE, Kantorow M, Cvekl A (2010) Efficient generation of lens progenitor cells and lentoid bodies from human embryonic stem cells in chemically defined conditions. FASEB J 24:3274–3283

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM (2006) Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281:15694–15700

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cell and Developmental Biology, University of Illinois, 601 S. Goodwin Avenue, Urbana, IL, 61801, USA

    Jonathan J. Henry, Alvin G. Thomas, Paul W. Hamilton, Lisa Moore & Kimberly J. Perry

Authors
  1. Jonathan J. Henry
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alvin G. Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul W. Hamilton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lisa Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kimberly J. Perry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan J. Henry .

Editor information

Editors and Affiliations

  1. Wistar Institute, Spruce Street 3601, Philadelphia, 19104, Pennsylvania, USA

    Ellen Heber-Katz

  2. Center for Regenerative Biology and, Medicine, Indiana University, North Blackford Street 402, Indianapolis, 46202, Indiana, USA

    David L. Stocum

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Henry, J.J., Thomas, A.G., Hamilton, P.W., Moore, L., Perry, K.J. (2012). Cell Signaling Pathways in Vertebrate Lens Regeneration. In: Heber-Katz, E., Stocum, D. (eds) New Perspectives in Regeneration. Current Topics in Microbiology and Immunology, vol 367. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2012_289

Download citation

Publish with us

Policies and ethics

Search

Navigation