ATRAID regulates the action of nitrogen-containing bisphosphonates on bone

Lauren E. Surface; Damon T. Burrow; Jinmei Li; Jiwoong Park; Sandeep Kumar; Cheng Lyu; Niki Song; Zhou Yu; Abbhirami Rajagopal; Yangjin Bae; Brendan H. Lee; Steven Mumm; Charles C. Gu; Jonathan C. Baker; Mahshid Mohseni; Melissa Sum; Margaret Huskey; Shenghui Duan; Vinieth N. Bijanki; Roberto Civitelli; Michael J. Gardner; Chris M. McAndrew; William M. Ricci; Christina A. Gurnett; Kathryn Diemer; Fei Wan; Christina L. Costantino; Kristen M. Shannon; Noopur Raje; Thomas B. Dodson; Daniel A. Haber; Jan E. Carette; Malini Varadarajan; Thijn R. Brummelkamp; Kivanc Birsoy; David M. Sabatini; Gabe Haller; Timothy R. Peterson

doi:10.1126/scitranslmed.aav9166

Research ArticleBone

ATRAID regulates the action of nitrogen-containing bisphosphonates on bone

View ORCID ProfileLauren E. Surface ¹,*,
View ORCID ProfileDamon T. Burrow²,
View ORCID ProfileJinmei Li²,
View ORCID ProfileJiwoong Park²,
View ORCID ProfileSandeep Kumar²,
View ORCID ProfileCheng Lyu²,
View ORCID ProfileNiki Song²,
Zhou Yu¹,†,
Abbhirami Rajagopal ³,‡,
View ORCID ProfileYangjin Bae³,
View ORCID ProfileBrendan H. Lee ³,
View ORCID ProfileSteven Mumm²,⁴,
View ORCID ProfileCharles C. Gu⁵,
View ORCID ProfileJonathan C. Baker⁶,
Mahshid Mohseni²,
Melissa Sum⁷,
Margaret Huskey²,
View ORCID ProfileShenghui Duan²,
View ORCID ProfileVinieth N. Bijanki⁴,
View ORCID ProfileRoberto Civitelli²,
Michael J. Gardner⁸,
View ORCID ProfileChris M. McAndrew⁹,
William M. Ricci¹⁰,
View ORCID ProfileChristina A. Gurnett⁹,¹¹,
View ORCID ProfileKathryn Diemer²,
View ORCID ProfileFei Wan¹²,
View ORCID ProfileChristina L. Costantino¹³,
Kristen M. Shannon¹⁴,
Noopur Raje¹⁴,
View ORCID ProfileThomas B. Dodson¹⁵,§,
View ORCID ProfileDaniel A. Haber ¹⁴,¹⁶,
Jan E. Carette¹⁷,
View ORCID ProfileMalini Varadarajan¹⁸,
View ORCID ProfileThijn R. Brummelkamp¹⁹,²⁰,²¹,
View ORCID ProfileKivanc Birsoy²²,
View ORCID ProfileDavid M. Sabatini ¹⁶,²³,²⁴,²⁵,
View ORCID ProfileGabe Haller¹¹,²⁶ and
View ORCID ProfileTimothy R. Peterson ²,²⁷,²⁸,||

¹Department of Molecular and Cellular Biology, Department of Chemistry and Chemical Biology, Faculty of Arts and Sciences Center for Systems Biology, Harvard University, Cambridge, MA 02138, USA.
²Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.
³Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.
⁴Center for Metabolic Bone Disease and Molecular Research, Shriners Hospital for Children, St. Louis, MO 63110, USA.
⁵Division of Biostatistics, Washington University School of Medicine, 660 S. Euclid Ave., Campus Box 8067, St. Louis, MO 63110, USA.
⁶Mallinckrodt Institute of Radiology, Washington University School of Medicine, 510 S. Kingshighway Blvd., St. Louis, MO 63110, USA.
⁷Division of Endocrinology, Diabetes and Metabolism, NYU Langone Health, 530 1st Ave., Schwartz 5E., New York, NY 10016, USA.
⁸Department of Orthopedic Surgery, Stanford University, 450 Broadway Street, Redwood City, CA 94063, USA.
⁹Department of Orthopedic Surgery, Washington University School of Medicine, 4938 Parkview Place, St. Louis, MO 63110, USA.
¹⁰Hospital for Special Surgery Main Campus–Belaire Building, 525 East 71st Street 2nd Floor, New York, NY 10021, USA.
¹¹Department of Neurology, Washington University School of Medicine, Campus Box 8111, 660 S. Euclid Ave., St. Louis, MO 63110, USA.
¹²Department of Surgery, Washington University School of Medicine, Campus Box 8109, 4590 Children’s Place, Suite 9600, St. Louis, MO 63110, USA.
¹³Massachusetts General Hospital Cancer Center and Department of Surgery, Harvard Medical School, Boston, MA 02114, USA.
¹⁴Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA 02114, USA.
¹⁵Department of Oral and Maxillofacial Surgery, Massachusetts General Hospital and Harvard School of Dental Medicine, Boston, MA 02114, USA.
¹⁶Howard Hughes Medical Institute (HHMI), Chevy Chase, MD 20815, USA.
¹⁷Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305, USA.
¹⁸Oncology Disease Area, Novartis Institutes for BioMedical Research, Cambridge, CA 02140, USA.
¹⁹Oncode Institute, Division of Biochemistry, The Netherlands Cancer Institute, Plesmanlaan 121, 1066CX Amsterdam, Netherlands.
²⁰CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, 1090 Vienna, Austria.
²¹Cancer Genomics Center, Plesmanlaan 121, 1066CX Amsterdam, Netherlands.
²²The Rockefeller University, 1230 York Ave., New York, NY 10065, USA.
²³Whitehead Institute, 9 Cambridge Center, Cambridge, MA 02139, USA.
²⁴Department of Biology, Massachusetts Institute of Technology (MIT), 77 Massachusetts Avenue, Cambridge, MA 02139, USA.
²⁵David H. Koch Center for Integrative Cancer Research at MIT, 77 Massachusetts Avenue, Cambridge, MA 02139, USA.
²⁶Department of Neurosurgery, Washington University School of Medicine, Campus Box 8057, 660 S. Euclid Ave., St. Louis, MO 63110, USA.
²⁷Department of Genetics, Washington University School of Medicine, 4515 McKinley Ave. Campus Box 8232, St. Louis, MO 63110, USA.
²⁸Institute for Public Health, Washington University School of Medicine, 600 S. Taylor Suite 2400, Campus Box 8217, St. Louis, MO 63110, USA.

↵||Corresponding author. Email: timrpeterson{at}wustl.edu

↵* Present address: Endocrine Unit, 55 Fruit St., Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
↵† Present address: Howard Hughes Medical Institute (HHMI) Janelia Research Campus, 19700 Helix Drive, Ashburn, VA 20147, USA.
↵‡ Present address: Harris County Public Health, Houston, TX 77027, USA.
↵§ Present address: Department of Oral and Maxillofacial Surgery, University of Washington School of Dentistry, Seattle, WA 98195, USA.

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Science Translational Medicine 20 May 2020:
Vol. 12, Issue 544, eaav9166
DOI: 10.1126/scitranslmed.aav9166

Lauren E. Surface

1Department of Molecular and Cellular Biology, Department of Chemistry and Chemical Biology, Faculty of Arts and Sciences Center for Systems Biology, Harvard University, Cambridge, MA 02138, USA.

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Damon T. Burrow

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Jinmei Li

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Jiwoong Park

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Sandeep Kumar

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Cheng Lyu

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Niki Song

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Zhou Yu

1Department of Molecular and Cellular Biology, Department of Chemistry and Chemical Biology, Faculty of Arts and Sciences Center for Systems Biology, Harvard University, Cambridge, MA 02138, USA.

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Abbhirami Rajagopal

3Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

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Yangjin Bae

3Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

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Brendan H. Lee

3Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

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Steven Mumm

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

4Center for Metabolic Bone Disease and Molecular Research, Shriners Hospital for Children, St. Louis, MO 63110, USA.

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Charles C. Gu

5Division of Biostatistics, Washington University School of Medicine, 660 S. Euclid Ave., Campus Box 8067, St. Louis, MO 63110, USA.

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Jonathan C. Baker

6Mallinckrodt Institute of Radiology, Washington University School of Medicine, 510 S. Kingshighway Blvd., St. Louis, MO 63110, USA.

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Mahshid Mohseni

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Melissa Sum

7Division of Endocrinology, Diabetes and Metabolism, NYU Langone Health, 530 1st Ave., Schwartz 5E., New York, NY 10016, USA.

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Margaret Huskey

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Shenghui Duan

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Vinieth N. Bijanki

4Center for Metabolic Bone Disease and Molecular Research, Shriners Hospital for Children, St. Louis, MO 63110, USA.

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Roberto Civitelli

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Michael J. Gardner

8Department of Orthopedic Surgery, Stanford University, 450 Broadway Street, Redwood City, CA 94063, USA.

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Chris M. McAndrew

9Department of Orthopedic Surgery, Washington University School of Medicine, 4938 Parkview Place, St. Louis, MO 63110, USA.

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William M. Ricci

10Hospital for Special Surgery Main Campus–Belaire Building, 525 East 71st Street 2nd Floor, New York, NY 10021, USA.

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Christina A. Gurnett

9Department of Orthopedic Surgery, Washington University School of Medicine, 4938 Parkview Place, St. Louis, MO 63110, USA.

11Department of Neurology, Washington University School of Medicine, Campus Box 8111, 660 S. Euclid Ave., St. Louis, MO 63110, USA.

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Kathryn Diemer

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

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Fei Wan

12Department of Surgery, Washington University School of Medicine, Campus Box 8109, 4590 Children’s Place, Suite 9600, St. Louis, MO 63110, USA.

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Christina L. Costantino

13Massachusetts General Hospital Cancer Center and Department of Surgery, Harvard Medical School, Boston, MA 02114, USA.

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Kristen M. Shannon

14Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA 02114, USA.

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Noopur Raje

14Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA 02114, USA.

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Thomas B. Dodson

15Department of Oral and Maxillofacial Surgery, Massachusetts General Hospital and Harvard School of Dental Medicine, Boston, MA 02114, USA.

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Daniel A. Haber

14Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA 02114, USA.

16Howard Hughes Medical Institute (HHMI), Chevy Chase, MD 20815, USA.

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Jan E. Carette

17Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305, USA.

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Malini Varadarajan

18Oncology Disease Area, Novartis Institutes for BioMedical Research, Cambridge, CA 02140, USA.

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Thijn R. Brummelkamp

19Oncode Institute, Division of Biochemistry, The Netherlands Cancer Institute, Plesmanlaan 121, 1066CX Amsterdam, Netherlands.

20CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, 1090 Vienna, Austria.

21Cancer Genomics Center, Plesmanlaan 121, 1066CX Amsterdam, Netherlands.

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Kivanc Birsoy

22The Rockefeller University, 1230 York Ave., New York, NY 10065, USA.

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David M. Sabatini

16Howard Hughes Medical Institute (HHMI), Chevy Chase, MD 20815, USA.

23Whitehead Institute, 9 Cambridge Center, Cambridge, MA 02139, USA.

24Department of Biology, Massachusetts Institute of Technology (MIT), 77 Massachusetts Avenue, Cambridge, MA 02139, USA.

25David H. Koch Center for Integrative Cancer Research at MIT, 77 Massachusetts Avenue, Cambridge, MA 02139, USA.

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Gabe Haller

11Department of Neurology, Washington University School of Medicine, Campus Box 8111, 660 S. Euclid Ave., St. Louis, MO 63110, USA.

26Department of Neurosurgery, Washington University School of Medicine, Campus Box 8057, 660 S. Euclid Ave., St. Louis, MO 63110, USA.

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Timothy R. Peterson

2Division of Bone and Mineral Diseases, Department of Medicine, Washington University School of Medicine, BJC Institute of Health, 425 S. Euclid Ave., St. Louis, MO 63110, USA.

27Department of Genetics, Washington University School of Medicine, 4515 McKinley Ave. Campus Box 8232, St. Louis, MO 63110, USA.

28Institute for Public Health, Washington University School of Medicine, 600 S. Taylor Suite 2400, Campus Box 8217, St. Louis, MO 63110, USA.

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For correspondence: timrpeterson@wustl.edu

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ATRAID regulates the action of nitrogen-containing bisphosphonates on bone

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