Expression of the heparan sulfate 6-O-endosulfatases, Sulf1 and Sulf2, in the avian and mammalian inner ear suggests a role for sulfation during inner ear development
[en] Background: Inner ear morphogenesis is tightly regulated by the temporally and spatially coordinated action of signaling ligands and their receptors. Ligand-receptor interactions are influenced by heparan sulfate proteoglycans (HSPGs), cell surface molecules that consist of glycosaminoglycan chains bound to a protein core. Diversity in the sulfation pattern within glycosaminoglycan chains creates binding sites for numerous cell signaling factors, whose activities and distribution are modified by their association with HSPGs. Results: Here we describe the expression patterns of two extracellular 6-O-endosulfatases, Sulf1 and Sulf2, whose activity modifies the 6-O-sulfation pattern of HSPGs. We use in situ hybridization to determine the temporal and spatial distribution of transcripts during the development of the chick and mouse inner ear. We also use immunocytochemistry to determine the cellular localization of Sulf1 and Sulf2 within the sensory epithelia. Furthermore, we analyze the organ of Corti in Sulf1/Sulf2 double knockout mice and describe an increase in the number of mechanosensory hair cells. Conclusions: Our results suggest that the tuning of intracellular signaling, mediated by Sulf activity, plays an important role in the development of the inner ear.
Expression of the heparan sulfate 6-O-endosulfatases, Sulf1 and Sulf2, in the avian and mammalian inner ear suggests a role for sulfation during inner ear development
Publication date :
2015
Journal title :
Developmental Dynamics
ISSN :
1058-8388
eISSN :
1097-0177
Publisher :
Wiley Liss, Inc., New York, United States - New York
Adam J, Myat A, Le Roux I, Eddison M, Henrique D, Ish-Horowicz D, Lewis J. 1998. Cell fate choices and the expression of Notch, Delta and Serrate homologues in the chick inner ear: parallels with Drosophila sense-organ development. Development 125:4645-4654.
Ai X, Do A-T, Kusche-Gullberg M, Lindahl U, Lu K, Emerson CP. 2006. Substrate specificity and domain functions of extracellular heparan sulfate 6-O-endosulfatases, QSulf1 and QSulf2. J Biol Chem 281:4969-4976.
Ai X, Do A-T, Lozynska O, Kusche-Gullberg M, Lindahl U, Emerson CP. 2003. QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J Cell Biol 162:341-351.
Ai X, Kitazawa T, Do A-T, Kusche-Gullberg M, Labosky PA, Emerson CP. 2007. SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation. Development 134:3327-3338.
Bermingham NA, Hasan BA, Price SD, Vollrath MA, Ben-Arie N, Eatock RA, Bellen HJ, Lysakowski A, Zoghbi HY. 1999. Math1: an essential gene for the generation of inner ear hair cells. Science 284:1837-1841.
Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729-777.
Bissonnette JP, Fekete DM. 1996. Standard atlas of the gross anatomy of the developing inner ear of the chicken. J Comp Neurol 368:620-630.
Braquart-Varnier C, Danesin C, Clouscard-Martinato C, Agius E, Escalas N, Benazeraf B, Ai X, Emerson C, Cochard P, Soula C. 2004. A subtractive approach to characterize genes with regionalized expression in the gliogenic ventral neuroepithelium: identification of chick sulfatase 1 as a new oligodendrocyte lineage gene. Mol Cell Neurosci 25:612-628.
Chambers D, Mason I. 2000. Expression of sprouty2 during early development of the chick embryo is coincident with known sites of FGF signalling. Mech Dev 91:361-364.
Chang W, Lin Z, Kulessa H, Hebert J, Hogan BLM, Wu DK. 2008. Bmp4 is essential for the formation of the vestibular apparatus that detects angular head movements. PLoS Genet 4:e1000050.
Chapman E, Best MD, Hanson SR, Wong C-H. 2004. Sulfotransferases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew Chem Int Ed Engl 43:3526-3548.
Chen P, Johnson JE, Zoghbi HY, Segil N. 2002. The role of Math1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129:2495-2505.
Danesin C, Agius E, Escalas N, Ai X, Emerson C, Cochard P, Soula C. 2006. Ventral neural progenitors switch toward an oligodendroglial fate in response to increased Sonic hedgehog (Shh) activity: involvement of Sulfatase 1 in modulating Shh signaling in the ventral spinal cord. J Neurosci 26:5037-5048.
Daudet N, Ariza-McNaughton L, Lewis J. 2007. Notch signalling is needed to maintain, but not to initiate, the formation of prosensory patches in the chick inner ear. Development 134:2369-2378.
Daudet N, Lewis J. 2005. Two contrasting roles for Notch activity in chick inner ear development: specification of prosensory patches and lateral inhibition of hair-cell differentiation. Development 132:541-551.
Dhoot GK, Gustafsson MK, Ai X, Sun W, Standiford DM, Emerson CP. 2001. Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293:1663-1666.
Freeman SD, Moore WM, Guiral EC, Holme AD, Turnbull JE, Pownall ME. 2008. Extracellular regulation of developmental cell signaling by XtSulf1. Dev Biol 320:436-445.
Freter S, Muta Y, Mak SS, Rinkwitz S, Ladher RK. 2008. Progressive restriction of otic fate: the role of FGF and Wnt in resolving inner ear potential. Development. 135:3415-3424.
García-López R, Soula C, Martínez S. 2009. Expression analysis of Sulf1 in the chick forebrain at early and late stages of development. Dev Dyn 238:2418-2429.
Goodyear R, Holley M, Richardson G. 1995. Hair and supporting-cell differentiation during the development of the avian inner ear. J Comp Neurol 351:81-93.
Gorsi B, Liu F, Ma X, Chico TJA, Shrinivasan A, Kramer KL, Bridges E, Monteiro R, Harris AL, Patient R, Stringer SE. 2014. The heparan sulfate editing enzyme Sulf1 plays a novel role in zebrafish VegfA mediated arterial venous identity. Angiogenesis 17:77-91.
Gorsi B, Whelan S, Stringer SE. 2010. Dynamic expression patterns of 6-O endosulfatases during zebrafish development suggest a subfunctionalisation event for sulf2. Dev Dyn 239:3312-3323.
Groves AK, Fekete DM. 2012. Shaping sound in space: the regulation of inner ear patterning. Development 139:245-257.
Guiral EC, Faas L, Pownall ME. 2010. Neural crest migration requires the activity of the extracellular sulphatases XtSulf1 and XtSulf2. Dev Biol 341:375-388.
Hayashi T, Cunningham D, Bermingham-McDonogh O. 2007. Loss of Fgfr3 leads to excess hair cell development in the mouse organ of Corti. Dev Dyn 236:525-533.
Hayashi T, Ray CA, Bermingham-McDonogh O. 2008. Fgf20 is required for sensory epithelial specification in the developing cochlea. J Neurosci 28:5991-5999.
Heller S, Sheane CA, Javed Z, Hudspeth AJ. 1998. Molecular markers for cell types of the inner ear and candidate genes for hearing disorders. Proc Natl Acad Sci U S A 95:11400-11405.
Jayasena CS, Ohyama T, Segil N, Groves AK. 2008. Notch signaling augments the canonical Wnt pathway to specify the size of the otic placode. Development 135:2251-2261.
Kamimura K, Rhodes JM, Ueda R, McNeely M, Shukla D, Kimata K, Spear PG, Shworak NW, Nakato H. 2004. Regulation of Notch signaling by Drosophila heparan sulfate 3-O sulfotransferase. J Cell Biol 166:1069-1079.
Kusche-Gullberg M, Kjellén L. 2003. Sulfotransferases in glycosaminoglycan biosynthesis. Curr Opin Struct Biol 13:605-611.
Ladher RK, Wright TJ, Moon AM, Mansour SL, Schoenwolf GC. 2005. FGF8 initiates inner ear induction in chick and mouse. Genes Dev 19:603-613.
Lai J-P, Chien J, Strome SE, Staub J, Montoya DP, Greene EL, Smith DI, Roberts LR, Shridhar V. 2004. HSulf-1 modulates HGF-mediated tumor cell invasion and signaling in head and neck squamous carcinoma. Oncogene 23:1439-1447.
Lanford PJ, Lan Y, Jiang R, Lindsell C, Weinmaster G, Gridley T, Kelley MW. 1999. Notch signalling pathway mediates hair cell development in mammalian cochlea. Nat Genet 21:289-292.
Ledin J, Staatz W, Li J-P, Götte M, Selleck S, Kjellén L, Spillmann D. 2004. Heparan sulfate structure in mice with genetically modified heparan sulfate production. J Biol Chem 279:42732-42741.
Lin X. 2004. Functions of heparan sulfate proteoglycans in cell signaling during development. Development 131:6009-6021.
Lindahl U, Kusche-Gullberg M, Kjellén L. 1998. Regulated diversity of heparan sulfate. J Biol Chem 273:24979-24982.
Meyers JR, Planamento J, Ebrom P, Krulewitz N, Wade E, Pownall ME. 2013. Sulf1 modulates BMP signaling and is required for somite morphogenesis and development of the horizontal myoseptum. Dev Biol 378:107-121.
Morimoto-Tomita M, Uchimura K, Werb Z, Hemmerich S, Rosen SD. 2002. Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J Biol Chem 277:49175-49185.
Nagamine S, Koike S, Keino-Masu K, Masu M. 2005. Expression of a heparan sulfate remodeling enzyme, heparan sulfate 6-O-endosulfatase sulfatase FP2, in the rat nervous system. Brain Res Dev Brain Res 159:135-143.
Nagamine S, Tamba M, Ishimine H, Araki K, Shiomi K, Okada T, Ohto T, Kunita S, Takahashi S, Wismans RGP, van Kuppevelt TH, Masu M, Keino-Masu K. 2012. Organ-specific sulfation patterns of heparan sulfate generated by extracellular sulfatases Sulf1 and Sulf2 in mice. J Biol Chem 287:9579-9590.
Ohta S, Mansour SL, Schoenwolf GC. 2010. BMP/SMAD signaling regulates the cell behaviors that drive the initial dorsal-specific regional morphogenesis of the otocyst. Dev Biol 347:369-381.
Ohto T, Uchida H, Yamazaki H, Keino-Masu K, Matsui A, Masu M. 2002. Identification of a novel nonlysosomal sulphatase expressed in the floor plate, choroid plexus and cartilage. Genes Cells 7:173-185.
Ohyama T. 2006. Wnt signals mediate a fate decision between otic placode and epidermis. Development 133:865-875.
Ohyama T, Groves AK, Martin K. 2007. The first steps towards hearing: mechanisms of otic placode induction. Int J Dev Biol 51:463-472.
Ohyama T, Basch ML, Mishina Y, Lyons KM, Segil N, Groves AK. 2010. BMP signaling is necessary for patterning the sensory and nonsensory regions of the developing mammalian cochlea. J Neurosci 30:15044-15051.
Ono K, Kita T, Sato S, O'Neill P, Mak S-S, Paschaki M, Ito M, Gotoh N, Kawakami K, Sasai Y, Ladher RK. 2014. FGFR1-Frs2/3 signalling maintains sensory progenitors during inner ear hair cell formation. PLoS Genet 10:e1004118.
Ornitz DM. 2000. FGFs, heparan sulfate and FGFRs: complex interactions essential for development. Bioessays 22:108-112.
Pirvola U, Ylikoski J, Trokovic R, Hébert JM, McConnell SK, Partanen J. 2002. FGFR1 is required for the development of the auditory sensory epithelium. Neuron 35:671-680.
Pisconti A, Cornelison DD, Olguin HC, Antwine TL, Olwin BB. 2010. Syndecan-3 and Notch cooperate in regulating adult myogenesis. J Cell Biol 190:427-441.
Ratzka A, Kalus I, Moser M, Dierks T, Mundlos S, Vortkamp A. 2008. Redundant function of the heparan sulfate 6-O-endosulfatases Sulf1 and Sulf2 during skeletal development. Dev Dyn 237:339-353.
Ratzka A, Mundlos S, Vortkamp A. 2010. Expression patterns of sulfatase genes in the developing mouse embryo. Dev Dyn 239:1779-1788.
Riccomagno MM, Martinu L, Mulheisen M, Wu DK, Epstein DJ. 2002. Specification of the mammalian cochlea is dependent on Sonic Hedgehog. Genes Dev 16:2365-2378.
Riccomagno MM, Takada S, Epstein DJ. 2005. Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh. Genes Dev 19:1612-1623.
Torihara K, Morimitsu T, Suganuma T. 1995. Anionic sites on Reissner's membrane, stria vascularis, and spiral prominence. J Histochem Cytochem 43:299-305.
Torihara K, Suganuma T, Ide S, Morimitsu T. 1994. Anionic sites in blood capillaries of the mouse cochlear duct. Hear Res 77:69-74.
Tsuprun V, Santi P. 2001. Proteoglycan arrays in the cochlear basement membrane. Hear Res 157:65-76.
Turnbull J, Powell A, Guimond S. 2001. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol 11:75-82.
Wang S, Ai X, Freeman SD, Pownall ME, Lu Q, Kessler DS, Emerson CP. 2004. QSulf1, a heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis. Proc Natl Acad Sci U S A 101:4833-4838.
Winterbottom EF, Pownall ME. 2009. Complementary expression of HSPG 6-O-endosulfatases and 6-O-sulfotransferase in the hindbrain of Xenopus laevis. Gene Expr Patterns 9:166-172.
