Acid mucopolysaccharides in the eyes of the butterfly, Pieris brassicae and the moth, Philosamia ricini

  • Bendang Ao Department of Zoology, School of Sciences, Nagaland University, Lumami - 798627, Nagaland, India
  • Sentimenla Department of Zoology, School of Sciences, Nagaland University, Lumami - 798627, Nagaland, India
Keywords: Mucopolysaccharides, Rhabdome

Abstract

Mucopolysaccharides were detected by histochemical methods in the crystalline cones of both the butterfly (Pieris brassicae) and the moth (Philosamia ricini) commonly known as large cabbage white and eri silk moth respectively, but they were absent in the rhabdome part of both the insects. The mucopolysaccharides were extracted by biochemical method and the subsequent electrophoretic analysis revealed that they were similar to chondroitin 4 – sulfate. Moreover, chromatographic analysis revealed different sugar components in the eyes of the two insects. It is concluded that acid mucopolysaccharides have structural and other physiological roles in the visual apparatus but no part in light and dark or photoperiodic adaptations.

References

Achur RN, Muthusamy A, Madhunapantula SV, Bhavanandan VP, Seudieu Cand Gowda DC. 2004. Chondroitin sulfate proteoglycans of bovine cornea: structural characterization and assessment for the adherence of Plasmodium falciparum-infected erythrocytes. Biochem. Biophsy. Acta. 1701(1-2):109- 119.

Anseth A. 1961. Studies on corneal polysaccharides*: 111. Topographic and comparative biochemistry. Exp. Eye. Res. 1(2): 106 - 115.

Anseth A and Fransson LA. 1969. Studies on corneal polysaccharides*: V1. Isolation of dermatan sulfate from corneal scar tissue. Expl. Eye. Res. 8(3): 302 - 309.

Anseth A and Fransson LA. 1970. The importance of the polysaccharides for the normal function of the corneal stroma. Acta. Ophthal. 48(3): 455 - 464.

Balazs EA. 1965. Amino sugar-containing macromolecules in tissues of the eye and ear. In: The amino sugars. Balazs EA and Jeanloz RW, Eds. Vol 2A, 401 - 460. Academic press, New York.

Benedek GB. 1971. Theory of transparency of the eye. Appl. Optics. 10(3): 459 – 473.

Berman ER and Bach G. 1968. The acid mucopolysaccharides of cattle retina. Biochem. J. 108(part 1): 75 - 88.

Berman ER. 1969. Mucopolysaccharides (glycosaminoglycans) of the retina. Identification, distribution and possible biological role. Biol. Ophthalmol. 79: 5 - 31.

Bettelheim FA and Plessy B. 1975. The hydration of proteoglycans of bovine cornea. Biochem. Biophys. Acta. 381(1): 203 - 214.

Blochberger TC, Vergnes JP, Hempel J and Hassell JR. 1992. cDNA to chick lumican (Corneal keratan sulfate proteoglycan) reveals homology to the small interstitial proteoglycan gene family and expression in muscle and intestine. J. Biol. Chem. 267 (1): 347 – 352.

Bonanno JA, Klyce SD and Cragoe EJ. 1989. Mechanism of chloride uptake in rabbit corneal epithelium. Am. J. Physiol. 257(2 pt 1): C290 - C296.

Bron AJ. 2001. The architecture of the corneal stroma. Br. J. Ophthalmol. 85(4): 379 - 381.

Bulow HE and Hobert O. 2006. The molecular diversity of glycosaminoglycans shapes animal development. Annu. Rev. Cell. Dev. Biol. 22: 375 - 407.

Candia OA. 1976. Fluid and Cl transport by the epithelium of the isolated frog cornea. Fedn. Proc. 35: 703.

Candia OA and Zamudio AC. 1995. Chloride-activated water permeability in the frog corneal epithelium. J. Membr. Biol. 143(3): 259 - 266.

Carney SL. 1986. Proteoglycans. In Carbohydrate analysis-a practical approach. Chaplin MF and Kennedy JF, Eds. Oxford University Press, New York.

Castoro JA, Bettelheim AA, Bettelheim FA. 1988. Water gradients across bovine cornea. Invest. Ophthamol. Vis. Sci. 29(6): 963 - 968.

Cavallotti C, Feher J, Pescosolido N and Sagnelli P. 2004. Glycosaminoglycans in human trabecular meshwork: age- related changes. Ophthalmic. Res. 36(4): 211 - 217.

Cejkova J and Brettschneider I. 1969. The effect of hydration of the rabbit cornea on the histochemical demonstration of acid mucopolysaccharides. Histochem. 17(4): 327 - 336.

Cole D. 1970. Aqueous and ciliary body. In: Biochemistry of the eye. Graymore CN, Ed. 105 - 171. Academic Press, London and New York.

Conrad AH, Zhang Y, Tasheva ES and Conrad GW. 2010. Proteomic analysis of potential keratan sulfate, chondroitin sulfate A, and hyaluronic acid molecular interactions. Invest Ophthalmol. Vis. Sci. 51(9): 4500 - 4515.

Conrad G, Hamilton C and Haynes E. 1977. Differences in glycosaminoglycans synthesized by fibroblast-like cells from chick cornea, heart and skin. J. Biol. Chem. 252(19): 6861 - 6870.

Corpuz LM, Funderburgh JL, Funderburgh ML, Bottomley GS, Prakash S and Conrad GW. 1996. Molecular cloning and tissue distribution of keratocan: bovine corneal keratan sulfate proteoglycan. 37A. J. Biol. Chem. 271(16): 9759 - 9763.

Coster L, Rosenberg LC, Van der Rest M and Poole AR. 1987. The dermatan sulfate proteoglycans of bovine sclera and their relationship to those articular cartilage. An immunological and biochemical study. J. Biol.Chem. 262(8): 3809 - 3812.

Cox JL, Farrell RA and Hart RW and Langham ME. 1970. The transparency of the mammalian cornea. J. Physiol (Lond). 210(3): 601 - 616.

Cristol SM, Edelhauser HF and Lynn MJ. 1992. A comparison of corneal stromal edema induced from the anterior or the posterior surface. Refract. Corneal. Surg. 8(3): 224 - 229.

Deb MK and Raghuvarman A. 1994. Glycosaminoglycan fractions in the cornea of two fishes. Curr. Sci. 67(12): 1020.

Dey S. 1976. Acid mucopolysaccharides in the lens cutice of insects. MSc dissertation. North Eastern Hill University, Shillong, Meghalaya, India.

Dey S. 1980. Studies on certain physiological and biochemical aspects of vision in some arthropods. Ph.D. Thesis. North Eastern Hill University, Shillong, Meghalaya, India.

Dey S, Raghuvarman A and Michael RG. 1978. Acid mucopolysaccharides in the lens cuticle of fresh water prawn, Macrobrachium birmanicum (Crustacea) and the marine horse shoe crab, Limulus polyphemus (Xiphosura) and their physiological significance. IV. All. India. Symp. On. Comp. Animal. Physiol. Endocrinol.

Dietrich CP, Sampaio LO and Toledo OMS. 1977. Preparation of a crude AMPs fraction from tissues with proteolytic enzymes. In: Methods of biochemical analysis. Glick D, Ed. Vol. 24, 284 - 285. Wiley, New York.

Farber SJ, and Schubert M. 1957. The binding of cations by chondroitin sulfate. J. Clin. Invest. 36(12):1715 - 1722.

Fitzsimmons TD, Fagerholm P, Harfstrand A and Schenholm M. 1992. Hyaluronic acid is in the rabbit cornea after excimer laser superficial keratectomy. Invest. Ophthalmol. Vis. Sci. 33(11): 3011 - 3016.

Freund DE, McCally RL, Farrell RA, Cristol SM, L'Hernault NL and Edelhauser HF. 1995. Ultrastructuure in the anterior and posterior stroma of perfused human and rabbit corneas. Relation to transparency. Invest. Opthalmol. Vis. Sci. 36(8): 1508 - 1523.

Fthenou E, Zafiropoulos A, Tsatsakis A, Stathopoulos A, Karamanos NK and Tzanakakis GN. 2006. Chondroitin sulfate A chains enhance platelet derived growth factor-mediated signalling in fibrosarcoma cells. Int. J. Biochem. Cell. Biol. 38(12): 2141 – 2150.

Fthenou E, Zafiropoulos A, Katonis P, Tsatsakis A, Karamanos NK and Tzanakakis GN. 2008. Chondroitin sulfate prevents platelets derived growth factor-mediated phosphorylation of PDGF-Rbeta in normal human fibroblasts severely impairing mitogenic responses. J. Cell. Biochem. 103(6): 1866 - 1876.

Funderburgh JL, Funderburgh ML, Mann MM, Prakash S and Conrad GW. 1996. Synthesis of corneal keratan sulfate proteoglycans by bovine Keratocytes in vitro. J. Biol. Chem. 271 (49): 31431 - 31436.

Giri KV and Nigam AN. 1954. Circular paper chromatography of carbohydrates. J. Indian. Inst. Sci . 36: 49-63.

Goes RM, Laicine EM, Porcionatto MA, Bonciani NH and Haddad A. 1999. Glycosaminoglycans in components of the rabbit eye: Synthesis and charcterization. Curr. Eye. Res. 19 (2): 146 – 153.

Gambaro G and Van Der Woude FJ. (2000). Glycosaminoglycans: Use in treatment of diabetic nephropathy. J. Am. Soc. Nephrol. 11(2): 359 - 368.

Groves ML, McKeon R, Werner E, Nagarsheth M, Meador W and English AW. 2005. Axon regeneration in peripheral nerves is enhanced by proteoglycan degradation. Exp. Neural. 195(2): 278 - 292.

Hall CW, Liebaers I, Di Natale P and Neufeld EF. 1978. Enzymic diagnosis of the genetic mucopolysaccharides storage disorders. Methods. Enzymol. 50: 439-456.

Hedbys BO. 1961. The role of polysaccharides in corneal swelling. Exp. Eye. Res. 1(1): 81 – 89.

Hedbys BO. 1963. Studies on the hydration of the corneal stroma. 1 - 20. Akademisk. Lund.

Humason GL. 1971. Animal tissue techniques. W. H. Freeman and Co. San Francisco.

Jaques LB. 1977. Determination of heparin and related sulfated mucopolysaccharides. In: Methods of biochemical analysis. 24 - 206. 24:203-312.

Jeanloz RW. 1970. Mucopolysaccharides of higher animals. In The carbohydrates. W.Pigman and Herp, D.Horton. Eds. Vol 2B. 589 - 625 Academic Press, New York.

Katchalsky A. 1964. Polyelectrolytes and their biological interactions. Biophysc. J. 4(1): 9 - 41.

Kato T, Nakayasu K, Ikegami K, Obara T, Kanayama T and Kanai A. 1999. Analysis of glycosaminoglycans in rabbit cornea after excimer laser keratectomy. Br. J.Ophthalmol., 83(5): 609 - 612.

Kennedy JF and White CA. 1983. Bioactive carbohydrates: In Chemistry, biochemistry and biology. 183. Ellis Horwood Limited. Halstead Press, New York, Brisbane, Chichester, Toronto.

Kikkawa Y and Hirayama K. 1970. Uneven swelling properties of the corneal stroma. Invest. Ophthalmol. 9(10): 735 - 741.

Kobayashi TK and Pedrini V. 1973. Proteoglycans- collagen interactions in human costal cartilage. Biochem. Biophys. Acta . 303(1):148 - 160.

Krishnan N. 1965. Occurance of acid mucopolysaccharides in the cuticle of the scorpion Palamneus swammerdami. Curr. Sci. 34(4): 120 - 121.

Lee D and Wilson G. 1981. Non-uniform swelling properties of the corneal stroma. Curr. Eye.Res. 1(8): 457 - 461.

Leitner, JG and Kerby, GP 1954. Staining of acid mucopolysaccharides after chromatography on filter paper. Biotechnic & Histochemistry. Vol. 29, No. 5, 257-259

Li W, Vergnes JP, Cornuet PK and Hassell JR. 1992. cDNA clone to chick corneal chondroitin dermatan sulfate proteoglycan reveals identity to decorin. Arch. Biochem. Biophys.296(1): 190 - 197.

Li Q, Park PW, Wilson CL and Parks WC. 2002. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and trans-epithelial efflux of neutrophils in acute lung injury. Cell. 111(5): 635 - 46.

Lutjen-Drecoll E, Schenholm M, Tamm E and Tengblad A. 1990. Visualization of hyaluronic acid in the anterior segment of rabbit and monkey eyes. Exp. Eye. Res. 51 (1): 55 - 63.

Manton KJ, Leong DFM, Cool SM and Nurcombe V. (2007). Disruption of heparan and chondroitin sulfate signaling enhances mesenchymal stem cell-derived osteogenic differentiation via bone morphogenetic protein signaling pathways. Stem Cells. 25(11): 2845 - 2854.

Matalon R, Arbogast B and Dorfman A. 1974 a. Deficiency of chondroitin sulfate ChS N-acetylgalactosamine 4-sulfate sulfatase in Maroteaux-Lamy syndrome. Biochem. Biophys. Res. Commun. 61: 1450-1457.

Mathews MB. 1959. Macromolecular properties of isomeric chondroitin sulfates. Biochem. Biophys. Acta. 35: 9 - 17.

Mathews MB. 1975. Connective Tissue-Macromolecular structure and evolution. Springer-Verlag, Berlin, Heidelberg, New York. 318 pages.

Matsuoka LY, Wortsman J, Kupchella CE, Eng A and Dietrich JE. 1982. Histochemical characterization of the cutaneous involvement of acromegaly. Arch. Intern. Med. 142 (10): 1820 - 1823.

Maurice DM and Riley MV. 1970. In: The biochemistry of the eye. Graymore CN, Ed. 1-95. Academic Press, London and New York.

Maurice DM. 1957. The structure and transparency of the cornea. J. Physiol (Lond). 136(2): 263 - 286.

Maurice DM. 1969. The cornea and sclera: In the eye. Davson H, 2nd Ed. Vol. 1, pp. 489-600. Academic Press, New York.

Maurice DM. 1972. The location of the fluid pump in the cornea. J. Physiol. London. 221(1): 43 - 54.

McAdams BD. and McLoon SC. 1995. Expression of chondroitin sulfate and keratan sulfate proteoglycans in the path of growing retinal axons in the developing chick. . 352 (4): 594 - 606.

McCally RL and Farrell RA. 1990. Light scattering from cornea and corneal transparency. In: Non invasive diagnostic techniques in ophthalmology. Masters BR, Ed . New York, Springer-Verlag. pp 189 - 210.

McKusick VA, Neufeld EF and Kelley TE. 1978. The mucopolysaccharides storage diseases. In : The metabolic basis of inherited disease. Stanbury JB, Wyngaarden J B. and Fredrickson, DS, 4th Eds. pp. 1282. McGraw-Hill, New York.

Meenakshi VR and Scheer BT. 1959. Acid mucopolysaccharides of the crustacean cuticle. Science. 130(3383): 1189 - 1190.

Meyer K. 1938. The chemistry and biology of mucopolysaccharides and glycoproteins. Cold Spring Harbor Symposia on Quantitative Biology. 6: 91-102.

Miao HQ, Ishai-Michaeli R, Atzmon R, Peretz T and Vodavsky I. 1996. Sulfate moieties in the subendothelial extracellular matrix are involved in basic fibroblast growth factor sequestration, dimerization, and stimulation of cell proliferation. J. Bio. Chem. 271(9): 4879 – 4886.

Mohan PS and Spiro RG. 1991. Characterization of heparan sulfate proteoglycan from calf lens capsule and proteoglycans synthesized by cultured lens epithelial cells. Comparison with other basement membrane proteoglycans. J. Biol. Chem. 266 (13): 8567 -8575.

Moczar E. and Moczar M. 1972. The phylogenetic evolution of the corneal stroma. Distribution of carbohydrates in the macromolecular complexes of the primate, Baboon (Cynocephalus papio- papio) corneal stroma. Comp. Biochem. Physiol. 43(2): 261 - 270.

Moczar M. and Moczar E. 1973. Phylogenetic evolution of the cornea. Macromolecular composition of the corneal stroma of the squid (Sepia officinalis). Comp. Biochem. Physiol. 45(1): 213 - 223.

Muller LJ, Pels E and Vrensen FJM 2001. The specific architecture of the anterior stroma accounts for maintenance of corneal curvature. Br. J. Ophthalmol. 85(4): 437 – 443.

Narula P, Xu M and Kuang KY, Akiyama R and Fischbarg J. 1992. Fluid transport across cultured bovine corneal endothelial cell monolayers. Am. J. Physiol. 262(1 pt 1): C98 - 103.

Neufeld EF and Fratantoni JC. 1970. Inborn errors of mucopolysaccharides metabolism. Science. 169(3941): 141-146. New York, London.

Ogston AG. 1966 a. On water binding. Federation. Proc. 25(3): 986 - 989.

Ogston AG. 1970. The biological function of the glycosaminoglycans. In: Chemistry and Molecular Biology of the intercellular matrix. Balazs, E. A. Ed. Vol. 3. pp. 1231 -1240. Academic Press, New York.

Ogston AG and Wells JD. 1972. The osmotic properties of sulphoethyl–sephadex. A model for cartilage. Biochem. J. 128(part 3): 685 - 690.

Olson SK, Bishop J R, Yates J R, Oegema K. and Esko JD. 2006. Identification of novel chondroitin proteoglycans in Caenorhabditis elegans : embryonic cell division depends on CPG-1 and CPG-2. J. Chem. Biol. 173 (6): 985 - 994.

Oosawa F. 1971. Polyelectrolytes. Dekker, New York.

Park PW, Pier GB, Hinkes MT and Bernfield M. 2001. Exploitation of syndecan-1 shedding by Pseudomonas aeruginosa enhances virulence. Nature. 411(6833): 98 - 102.

Payrau P, Pouliquen Y, Faure JP and Offret G. 1967. In : Biochemisty of the eye. Graymore, C. N. Ed. pp. 13. Academic press, London, New York.

Plaas AH, West LA, Thonar EJA, Karcioglu ZA, Smith CJ, Klintworth GK and Hascall VC. 2001. Altered fine structures of corneal and skeletal keratan sulfate and chondroitin/dermatan sulfate in macular corneal dystrophy. J. Biol. Chem. 276(43): 39788 - 39796.

Raghuvarman A, Dey S and Hermann HR Jr. 1998. Acid mucopolysaccharides in the body cuticle of the Peripatus, Typhiloperipatus weldoni in relation to the cutaneous mode of sperm transfer. J. Endocrinol. Reprod. 1 (2): 80 - 85.

Rhodes KE and Fawcett JW. 2004. Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J. Anat. 204(1): 33 - 48.

Robert I and Robert B. 1967. Structural glycoproteins of membranes and connective tissue: biochemical and immunopathological properties. In: H. PEETERS, (ed.), Protides of biological fluids, vol. is, p. 143. Amsterdam: Elsevier 1967.

Rubin PS and Horward JR. 1950. Conference on metabolic interactions. Trans. 2nd Conf. Col. 2. 155.

Schachtschabel DO, Bigalke B and Rohen JW. 1977. Production of glycosaminoglycans by cell cultures of the trabecular meshwork of the primate eye. Exp. Eye. Res. 24(1): 71 - 80.

Sertie AL, Sossi V, Camargo AA, Zatz M, Brahe C and Passos-Bueno MR. 2000. Collagen XV111, containing an endogenous inhibitor of angiogenesis and tumor growth, plays a critical role in the maintenance of retinal structure and in neural tube closure (Knobloch syndrome). Hum. Mol. Genet. 9(13): 2051 - 2058.

Sundara Rajulu G. 1969. Presence of acid mucopolysaccharides in the cuticle of a millipede, Cingalobolus bugnioni. Curr. Sci. 38(14): 345 - 346.

Tai GH, Nieduszynski IA, Fullwood NJ and Huckerby TN. 1997. Human corneal keratan sulfates. J. Biol. Chem. 272(45): 28227 - 28231.

Takahashi T, Cho HI, Kublin CL and Cintron C. 1993. Keratan sulfate and dermatan sulfate proteoglycans associate with type V1 collagen in fetal rabbit cornea. J. Histochem. Cytochem. 46 41(10): 1447 - 1457.

Trevelyan WE, Procter DP and Harrison JS. 1950. Detection of sugars on paper chromatograms. Nature. Lond. 166(4219): 444 - 445.

Urist MR, Speer DP, Ibsen KJ and Strates BS. 1968. Calcium binding by chondroitin sulfate. Calcif. Tissue. Res. 2(1): 253 - 261.

Van Horn DL, Doughman DJ, Harris JE, Miller GE, Lindstrom R and Good RA. 1975. Ultrastructure of human organ-cultured cornea. 11. Stroma and epithelium. Arch. Ophthalmol. 93(4): 275 - 277.

Wang L, Fuster M, Sriramarao P and Esko JD. 2005. Endothelial heparan sulfate deficiency impairs L-selectin and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat. Immunol. 6(9): 902 -910.

Wigglesworth VB. 1965. The principle of Insect Physiology. English Language book Society. Methuen and Co. Ltd. 25 - 47.

Yang H, Reinach PS, Koniarek JP, Wang Z, Iserovich P and Fischbarg J. 2000. Fluid transport by cultured corneal epithelial cell layers. Br. J. Ophthalmol. 84(2): 199 - 204.

Yue BY, Lin CC, Fei PF and Tso Mo 1984. Effects of chondroitin sulfate on metabolism of trabecular meshwork. Exp. Eye. Res. 38 (1): 35 - 44.
Published
2013-11-11
How to Cite
Ao, B., & Sentimenla. (2013). Acid mucopolysaccharides in the eyes of the butterfly, Pieris brassicae and the moth, Philosamia ricini. Journal of Research in Biology, 3(6), 1072-1085. Retrieved from https://ojs.jresearchbiology.com/ojs1/index.php/jrb/article/view/316