Cell surface glypicans are low-affinity endostatin receptors

S. Ananth Karumanchi; Vivekanand Jha; Ramani Ramchandran; Anil Karihaloo; Leonidas Tsiokas; Barden Chan; Mohanraj Dhanabal; Jun Ichi Hanai; Ganesh Venkataraman; Zachary Shriver; Nishla Keiser; Raghu Kalluri; Huiyan Zeng; Debabrata Mukhopadhyay; Robert L. Chen; Arthur D. Lander; Kazuki Hagihara; Yu Yamaguchi; Ram Sasisekharan; Lloyd Cantley; Vikas P. Sukhatme

doi:10.1016/S1097-2765(01)00225-8

Cell surface glypicans are low-affinity endostatin receptors

S. Ananth Karumanchi, Vivekanand Jha, Ramani Ramchandran, Anil Karihaloo, Leonidas Tsiokas, Barden Chan, Mohanraj Dhanabal, Jun Ichi Hanai, Ganesh Venkataraman, Zachary Shriver, Nishla Keiser, Raghu Kalluri, Huiyan Zeng, Debabrata Mukhopadhyay, Robert L. Chen, Arthur D. Lander, Kazuki Hagihara, Yu Yamaguchi, Ram Sasisekharan, Lloyd CantleyVikas P. Sukhatme

Jacksonville, FL

Research output: Contribution to journal › Article › peer-review

259 Scopus citations

Abstract

Endostatin, a collagen XVIII fragment, is a potent anti-angiogenic protein. We sought to identify its endothelial cell surface receptor(s). Alkaline phosphatase-tagged endostatin bound endothelial cells revealing two binding affinities. Expression cloning identified glypican, a cell surface proteoglycan as the lower-affinity receptor. Biochemical and genetic studies indicated that glypicans' heparan sulfate glycosaminoglycans were critical for endostatin binding. Furthermore, endostatin selected a specific octasulfated hexasaccharide from a sequence in heparin. We have also demonstrated a role for endostatin in renal tubular cell branching morphogenesis and show that glypicans serve as low-affinity receptors for endostatin in these cells, as in endothelial cells. Finally, antisense experiments suggest the critical importance of glypicans in mediating endostatin activities.

Original language	English (US)
Pages (from-to)	811-822
Number of pages	12
Journal	Molecular Cell
Volume	7
Issue number	4
DOIs	https://doi.org/10.1016/S1097-2765(01)00225-8
State	Published - Apr 2001

ASJC Scopus subject areas

Molecular Biology
Cell Biology

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10.1016/S1097-2765(01)00225-8

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Karumanchi, S. A., Jha, V., Ramchandran, R., Karihaloo, A., Tsiokas, L., Chan, B., Dhanabal, M., Hanai, J. I., Venkataraman, G., Shriver, Z., Keiser, N., Kalluri, R., Zeng, H., Mukhopadhyay, D., Chen, R. L., Lander, A. D., Hagihara, K., Yamaguchi, Y., Sasisekharan, R., ... Sukhatme, V. P. (2001). Cell surface glypicans are low-affinity endostatin receptors. Molecular Cell, 7(4), 811-822. https://doi.org/10.1016/S1097-2765(01)00225-8

Karumanchi, SA, Jha, V, Ramchandran, R, Karihaloo, A, Tsiokas, L, Chan, B, Dhanabal, M, Hanai, JI, Venkataraman, G, Shriver, Z, Keiser, N, Kalluri, R, Zeng, H, Mukhopadhyay, D, Chen, RL, Lander, AD, Hagihara, K, Yamaguchi, Y, Sasisekharan, R, Cantley, L & Sukhatme, VP 2001, 'Cell surface glypicans are low-affinity endostatin receptors', Molecular Cell, vol. 7, no. 4, pp. 811-822. https://doi.org/10.1016/S1097-2765(01)00225-8

@article{37b383e422df45d294cacd8ea33759f4,

title = "Cell surface glypicans are low-affinity endostatin receptors",

abstract = "Endostatin, a collagen XVIII fragment, is a potent anti-angiogenic protein. We sought to identify its endothelial cell surface receptor(s). Alkaline phosphatase-tagged endostatin bound endothelial cells revealing two binding affinities. Expression cloning identified glypican, a cell surface proteoglycan as the lower-affinity receptor. Biochemical and genetic studies indicated that glypicans' heparan sulfate glycosaminoglycans were critical for endostatin binding. Furthermore, endostatin selected a specific octasulfated hexasaccharide from a sequence in heparin. We have also demonstrated a role for endostatin in renal tubular cell branching morphogenesis and show that glypicans serve as low-affinity receptors for endostatin in these cells, as in endothelial cells. Finally, antisense experiments suggest the critical importance of glypicans in mediating endostatin activities.",

author = "Karumanchi, {S. Ananth} and Vivekanand Jha and Ramani Ramchandran and Anil Karihaloo and Leonidas Tsiokas and Barden Chan and Mohanraj Dhanabal and Hanai, {Jun Ichi} and Ganesh Venkataraman and Zachary Shriver and Nishla Keiser and Raghu Kalluri and Huiyan Zeng and Debabrata Mukhopadhyay and Chen, {Robert L.} and Lander, {Arthur D.} and Kazuki Hagihara and Yu Yamaguchi and Ram Sasisekharan and Lloyd Cantley and Sukhatme, {Vikas P.}",

note = "Funding Information: This work was funded by grants from the NIH to V. P. S., the Arnold and Mabel Beckman Foundation, the Burroughs Wellcome Foundation, and NIH to R. S., NIH to L. G. C., NIH KO8 to S. A. K., and an ISN fellowship award to V. J. We thank D. Liu, K. Pojasek, T. Daniel, M. Simons, R. Volk for help with reagents; S. Soker, B. Neel, S. Sokol, N. Shworak, S. Freedman, S. Alper, L. C. Cantley, F. H. Epstein, and members of the Sukhatme Laboratory for helpful discussions, and J. Barasch for personal communication.",

year = "2001",

month = apr,

doi = "10.1016/S1097-2765(01)00225-8",

language = "English (US)",

volume = "7",

pages = "811--822",

journal = "Molecular Cell",

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T1 - Cell surface glypicans are low-affinity endostatin receptors

AU - Karumanchi, S. Ananth

AU - Jha, Vivekanand

AU - Ramchandran, Ramani

AU - Karihaloo, Anil

AU - Tsiokas, Leonidas

AU - Chan, Barden

AU - Dhanabal, Mohanraj

AU - Hanai, Jun Ichi

AU - Venkataraman, Ganesh

AU - Shriver, Zachary

AU - Keiser, Nishla

AU - Kalluri, Raghu

AU - Zeng, Huiyan

AU - Mukhopadhyay, Debabrata

AU - Chen, Robert L.

AU - Lander, Arthur D.

AU - Hagihara, Kazuki

AU - Yamaguchi, Yu

AU - Sasisekharan, Ram

AU - Cantley, Lloyd

AU - Sukhatme, Vikas P.

N1 - Funding Information: This work was funded by grants from the NIH to V. P. S., the Arnold and Mabel Beckman Foundation, the Burroughs Wellcome Foundation, and NIH to R. S., NIH to L. G. C., NIH KO8 to S. A. K., and an ISN fellowship award to V. J. We thank D. Liu, K. Pojasek, T. Daniel, M. Simons, R. Volk for help with reagents; S. Soker, B. Neel, S. Sokol, N. Shworak, S. Freedman, S. Alper, L. C. Cantley, F. H. Epstein, and members of the Sukhatme Laboratory for helpful discussions, and J. Barasch for personal communication.

PY - 2001/4

Y1 - 2001/4

N2 - Endostatin, a collagen XVIII fragment, is a potent anti-angiogenic protein. We sought to identify its endothelial cell surface receptor(s). Alkaline phosphatase-tagged endostatin bound endothelial cells revealing two binding affinities. Expression cloning identified glypican, a cell surface proteoglycan as the lower-affinity receptor. Biochemical and genetic studies indicated that glypicans' heparan sulfate glycosaminoglycans were critical for endostatin binding. Furthermore, endostatin selected a specific octasulfated hexasaccharide from a sequence in heparin. We have also demonstrated a role for endostatin in renal tubular cell branching morphogenesis and show that glypicans serve as low-affinity receptors for endostatin in these cells, as in endothelial cells. Finally, antisense experiments suggest the critical importance of glypicans in mediating endostatin activities.

AB - Endostatin, a collagen XVIII fragment, is a potent anti-angiogenic protein. We sought to identify its endothelial cell surface receptor(s). Alkaline phosphatase-tagged endostatin bound endothelial cells revealing two binding affinities. Expression cloning identified glypican, a cell surface proteoglycan as the lower-affinity receptor. Biochemical and genetic studies indicated that glypicans' heparan sulfate glycosaminoglycans were critical for endostatin binding. Furthermore, endostatin selected a specific octasulfated hexasaccharide from a sequence in heparin. We have also demonstrated a role for endostatin in renal tubular cell branching morphogenesis and show that glypicans serve as low-affinity receptors for endostatin in these cells, as in endothelial cells. Finally, antisense experiments suggest the critical importance of glypicans in mediating endostatin activities.

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U2 - 10.1016/S1097-2765(01)00225-8

DO - 10.1016/S1097-2765(01)00225-8

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AN - SCOPUS:0035021908

SN - 1097-2765

VL - 7

SP - 811

EP - 822

JO - Molecular Cell

JF - Molecular Cell

IS - 4

ER -

Cell surface glypicans are low-affinity endostatin receptors

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