Biomarkers of cetuximab resistance in patients with head and neck squamous cell carcinoma

Olivia Leblanc; Sophie Vacher; Charlotte Lecerf; Emmanuelle Jeannot; Jerzy Klijanienko; Frédérique Berger; Caroline Hoffmann; Valentin Calugaru; Nathalie Badois; Anne Chilles; Maria Lesnik; Samar Krhili; Ivan Bieche; Christophe Le Tourneau; Maud Kamal

doi:10.20892/j.issn.2095-3941.2019.0153

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3. Soerjomataram I,
4. Dikshit R,
5. Eser S,
6. Mathers C,
7. Rebelo M, et al.
Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015; 136: E359–86.
OpenUrl CrossRef PubMed Web of Science
2.↵
2. Ang KK,
3. Harris J,
4. Wheeler R,
5. Weber R,
6. Rosenthal DI,
7. Nguyen-Tân PF, et al.
Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med. 1993; 22: 1718–1722.
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3.↵
2. Bonner JA,
3. Harari PM,
4. Giralt J,
5. Azarnia N,
6. Shin DM,
7. Cohen RB, et al.
Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med. 1993; 22: 1718–1722.
OpenUrl
4.↵
2. Vermorken JB,
3. Mesia R,
4. Rivera F,
5. Remenar E,
6. Kawecki A,
7. Rottey S, et al.
Platinum-based chemotherapy plus cetuximab in head and neck cancer. N Engl J Med. 1993; 22: 1718–1722.
OpenUrl
5.↵
2. Depenni R,
3. Cossu Rocca M,
4. Ferrari D,
5. Azzarello G,
6. Baldessari C,
7. Alù M, et al.
Clinical outcomes and prognostic factors in recurrent and/or metastatic head and neck cancer patients treated with chemotherapy plus cetuximab as first-line therapy in a real-world setting. Eur J Cancer. 1993; 22: 1718–1722.
OpenUrl
6.
2. Byrne K,
3. Hallworth P,
4. Monfared AAT,
5. Moshyk A,
6. Shaw JW.
Real-world systemic therapy treatment patterns for squamous cell carcinoma of the head and neck in Canada. Curr Oncol. 2019; 26: e167–74.
OpenUrl
7.
2. Nadler E,
3. Joo S,
4. Boyd M,
5. Black-Shinn J,
6. Chirovsky D.
Treatment patterns and outcomes among patients with recurrent/metastatic squamous cell carcinoma of the head and neck. Future Oncol. 1993; 22: 1718–1722.
OpenUrl
8.↵
2. Byrne K,
3. Zanotti G,
4. Hallworth P,
5. Roughley A,
6. Martini JF,
7. Uehara R, et al.
Real-world treatment patterns and outcomes of patients with stage IV squamous cell carcinoma of the head and neck. Future Oncol. 1993; 22: 1718–1722.
OpenUrl
9.↵
2. Licitra L,
3. Mesia R,
4. Rivera F,
5. Remenár É,
6. Hitt R,
7. Erfán J, et al.
Evaluation of EGFR gene copy number as a predictive biomarker for the efficacy of cetuximab in combination with chemotherapy in the first-line treatment of recurrent and/or metastatic squamous cell carcinoma of the head and neck: EXTREME study. Ann Oncol. 1993; 22: 1718–1722.
OpenUrl
10.↵
2. Bertotti A,
3. Sassi F.
Molecular pathways: sensitivity and resistance to anti-EGFR antibodies. Clin Cancer Res. 1993; 22: 1718–1722.
OpenUrl
11.↵
2. Bossi P,
3. Bergamini C,
4. Siano M,
5. Cossu Rocca M,
6. Sponghini AP,
7. Favales F, et al.
Functional genomics uncover the biology behind the responsiveness of head and neck squamous cell cancer patients to cetuximab. Clin Cancer Res. 1993; 22: 1718–1722.
OpenUrl
12.↵
The Cancer Genome Atlas Network. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature. 1993; 22: 1718–1722.
OpenUrl
13.↵
2. Sablin MP,
3. Dubot C,
4. Klijanienko J,
5. Vacher S,
6. Ouafi L,
7. Chemlali W, et al.
Identification of new candidate therapeutic target genes in head and neck squamous cell carcinomas. Oncotarget. 1993; 22: 1718–1722.
OpenUrl
14.↵
2. Karapetis CS,
3. Khambata-Ford S,
4. Jonker DJ,
5. O’Callaghan CJ,
6. Tu DS,
7. Tebbutt NC, et al.
K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med. 1993; 22: 1718–1722.
OpenUrl
15.↵
2. Lièvre A,
3. Bachet JB,
4. Le Corre D,
5. Boige V,
6. Landi B,
7. Emile JF, et al.
KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res. 1993; 22: 1718–1722.
OpenUrl
16.↵
2. de la Rochefordiere A,
3. Kamal M,
4. Floquet A,
5. Thomas L,
6. Petrow P,
7. Petit T, et al.
PIK3CA pathway mutations predictive of poor response following standard radiochemotherapy ± cetuximab in cervical cancer patients. Clin Cancer Res. 1993; 22: 1718–1722.
OpenUrl
17.↵
2. Bossi P,
3. Resteghini C,
4. Paielli N,
5. Licitra L,
6. Pilotti S,
7. Perrone F.
Prognostic and predictive value of EGFR in head and neck squamous cell carcinoma. Oncotarget. 1993; 22: 1718–1722.
OpenUrl
18.↵
2. García-Carracedo D,
3. Villaronga MÁ,
4. Álvarez-Teijeiro S,
5. Hermida-Prado F,
6. Santamaría I,
7. Allonca E, et al.
Impact of PI3K/AKT/mTOR pathway activation on the prognosis of patients with head and neck squamous cell carcinomas. Oncotarget. 1993; 22: 1718–1722.
OpenUrl
19.↵
2. Iglesias-Bartolome R,
3. Martin D,
4. Gutkind JS.
Exploiting the head and neck cancer oncogenome: widespread PI3K-mTOR pathway alterations and novel molecular targets. Cancer Discov. 1993; 22: 1718–1722.
OpenUrl
20.↵
2. Rosell R,
3. Moran T,
4. Queralt C,
5. Porta R,
6. Cardenal F,
7. Camps C, et al.
Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med. 1993; 22: 1718–1722.
OpenUrl
21.↵
2. Morgillo F,
3. Della Corte CM,
4. Fasano M,
5. Ciardiello F.
Mechanisms of resistance to EGFR-targeted drugs: lung cancer. ESMO Open. 2016; 1: e000060.
22.↵
2. Cizkova M,
3. Dujaric ME,
4. Lehmann-Che J,
5. Scott V,
6. Tembo O,
7. Asselain B, et al.
Outcome impact of PIK3CA mutations in HER2-positive breast cancer patients treated with trastuzumab. Br J Cancer. 1993; 22: 1718–1722.
OpenUrl
23.↵
2. Deguchi Y,
3. Okabe H,
4. Oshima N,
5. Hisamori S,
6. Minamiguchi S,
7. Muto M, et al.
PTEN loss is associated with a poor response to trastuzumab in HER2-overexpressing gastroesophageal adenocarcinoma. Gastric Cancer. 1993; 22: 1718–1722.
OpenUrl
24.↵
2. Nagata Y,
3. Lan KH,
4. Zhou XY,
5. Tan M,
6. Esteva FJ,
7. Sahin AA, et al.
PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell. 1993; 22: 1718–1722.
OpenUrl
25.
2. Berns K,
3. Horlings HM,
4. Hennessy BT,
5. Madiredjo M,
6. Hijmans EM,
7. Beelen K, et al.
A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell. 2007; 12: 395–402.
OpenUrl CrossRef PubMed Web of Science
26.↵
2. Esteva FJ,
3. Guo H,
4. Zhang SY,
5. Santa-Maria C,
6. Stone S,
7. Lanchbury JS, et al.
PTEN, PIK3CA, p-AKT, and p-p70S6K status: association with trastuzumab response and survival in patients with HER2-positive metastatic breast cancer. Am J Pathol. 1993; 22: 1718–1722.
OpenUrl
27.↵
2. Dave B,
3. Migliaccio I,
4. Gutierrez MC,
5. Wu MF,
6. Chamness GC,
7. Wong H, et al.
Loss of phosphatase and tensin homolog or phosphoinositol-3 kinase activation and response to trastuzumab or lapatinib in human epidermal growth factor receptor 2-overexpressing locally advanced breast cancers. J Clin Oncol. 1993; 22: 1718–1722.
OpenUrl
28.↵
2. Soria JC,
3. LoRusso P,
4. Bahleda R,
5. Lager J,
6. Liu L,
7. Jiang J, et al.
Phase I dose-escalation study of pilaralisib (SAR245408, XL147), a pan-class I PI3K inhibitor, in combination with erlotinib in patients with solid tumors. Oncologist. 1993; 22: 1718–1722.
OpenUrl
29.↵
2. Jänne PA,
3. Cohen RB,
4. Laird AD,
5. Macé S,
6. Engelman JA,
7. Ruiz-Soto R, et al.
Phase I safety and pharmacokinetic study of the PI3K/mTOR inhibitor SAR245409 (XL765) in combination with erlotinib in patients with advanced solid tumors. J Thorac Oncol. 1993; 22: 1718–1722.
OpenUrl
30.↵
2. Jimeno A,
3. Shirai K,
4. Choi M,
5. Laskin J,
6. Kochenderfer M,
7. Spira A, et al.
A randomized, phase II trial of cetuximab with or without PX-866, an irreversible oral phosphatidylinositol 3-kinase inhibitor, in patients with relapsed or metastatic head and neck squamous cell cancer. Ann Oncol. 1993; 22: 1718–1722.
OpenUrl

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External validation of prognostic and predictive gene signatures in head and neck cancer patients

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Keywords

[1] 1.↵

Ferlay J,
Soerjomataram I,
Dikshit R,
Eser S,
Mathers C,
Rebelo M, et al.
Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015; 136: E359–86.
OpenUrl CrossRef PubMed Web of Science

[3] Ferlay J,

[4] Soerjomataram I,

[5] Dikshit R,

[6] Eser S,

[7] Mathers C,

[8] Rebelo M, et al.

[9] 2.↵

Ang KK,
Harris J,
Wheeler R,
Weber R,
Rosenthal DI,
Nguyen-Tân PF, et al.
Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med. 1993; 22: 1718–1722.
OpenUrl

[11] Ang KK,

[12] Harris J,

[13] Wheeler R,

[14] Weber R,

[15] Rosenthal DI,

[16] Nguyen-Tân PF, et al.

[17] 3.↵

Bonner JA,
Harari PM,
Giralt J,
Azarnia N,
Shin DM,
Cohen RB, et al.
Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med. 1993; 22: 1718–1722.
OpenUrl

[19] Bonner JA,

[20] Harari PM,

[21] Giralt J,

[22] Azarnia N,

[23] Shin DM,

[24] Cohen RB, et al.

[25] 4.↵

Vermorken JB,
Mesia R,
Rivera F,
Remenar E,
Kawecki A,
Rottey S, et al.
Platinum-based chemotherapy plus cetuximab in head and neck cancer. N Engl J Med. 1993; 22: 1718–1722.
OpenUrl

[27] Vermorken JB,

[28] Mesia R,

[29] Rivera F,

[30] Remenar E,

[31] Kawecki A,

[32] Rottey S, et al.

[33] 5.↵

Depenni R,
Cossu Rocca M,
Ferrari D,
Azzarello G,
Baldessari C,
Alù M, et al.
Clinical outcomes and prognostic factors in recurrent and/or metastatic head and neck cancer patients treated with chemotherapy plus cetuximab as first-line therapy in a real-world setting. Eur J Cancer. 1993; 22: 1718–1722.
OpenUrl

[35] Depenni R,

[36] Cossu Rocca M,

[37] Ferrari D,

[38] Azzarello G,

[39] Baldessari C,

[40] Alù M, et al.

[41] 6.

Byrne K,
Hallworth P,
Monfared AAT,
Moshyk A,
Shaw JW.
Real-world systemic therapy treatment patterns for squamous cell carcinoma of the head and neck in Canada. Curr Oncol. 2019; 26: e167–74.
OpenUrl

[43] Byrne K,

[44] Hallworth P,

[45] Monfared AAT,

[46] Moshyk A,

[47] Shaw JW.

[48] 7.

Nadler E,
Joo S,
Boyd M,
Black-Shinn J,
Chirovsky D.
Treatment patterns and outcomes among patients with recurrent/metastatic squamous cell carcinoma of the head and neck. Future Oncol. 1993; 22: 1718–1722.
OpenUrl

[50] Nadler E,

[51] Joo S,

[52] Boyd M,

[53] Black-Shinn J,

[54] Chirovsky D.

[55] 8.↵

Byrne K,
Zanotti G,
Hallworth P,
Roughley A,
Martini JF,
Uehara R, et al.
Real-world treatment patterns and outcomes of patients with stage IV squamous cell carcinoma of the head and neck. Future Oncol. 1993; 22: 1718–1722.
OpenUrl

[57] Byrne K,

[58] Zanotti G,

[59] Hallworth P,

[60] Roughley A,

[61] Martini JF,

[62] Uehara R, et al.

[63] 9.↵

Licitra L,
Mesia R,
Rivera F,
Remenár É,
Hitt R,
Erfán J, et al.
Evaluation of EGFR gene copy number as a predictive biomarker for the efficacy of cetuximab in combination with chemotherapy in the first-line treatment of recurrent and/or metastatic squamous cell carcinoma of the head and neck: EXTREME study. Ann Oncol. 1993; 22: 1718–1722.
OpenUrl

[65] Licitra L,

[66] Mesia R,

[67] Rivera F,

[68] Remenár É,

[69] Hitt R,

[70] Erfán J, et al.

[71] 10.↵

Bertotti A,
Sassi F.
Molecular pathways: sensitivity and resistance to anti-EGFR antibodies. Clin Cancer Res. 1993; 22: 1718–1722.
OpenUrl

[73] Bertotti A,

[74] Sassi F.

[75] 11.↵

Bossi P,
Bergamini C,
Siano M,
Cossu Rocca M,
Sponghini AP,
Favales F, et al.
Functional genomics uncover the biology behind the responsiveness of head and neck squamous cell cancer patients to cetuximab. Clin Cancer Res. 1993; 22: 1718–1722.
OpenUrl

[77] Bossi P,

[78] Bergamini C,

[79] Siano M,

[80] Cossu Rocca M,

[81] Sponghini AP,

[82] Favales F, et al.

[83] 12.↵
The Cancer Genome Atlas Network. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature. 1993; 22: 1718–1722.
OpenUrl

[84] 13.↵

Sablin MP,
Dubot C,
Klijanienko J,
Vacher S,
Ouafi L,
Chemlali W, et al.
Identification of new candidate therapeutic target genes in head and neck squamous cell carcinomas. Oncotarget. 1993; 22: 1718–1722.
OpenUrl

[86] Sablin MP,

[87] Dubot C,

[88] Klijanienko J,

[89] Vacher S,

[90] Ouafi L,

[91] Chemlali W, et al.

[92] 14.↵

Karapetis CS,
Khambata-Ford S,
Jonker DJ,
O’Callaghan CJ,
Tu DS,
Tebbutt NC, et al.
K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med. 1993; 22: 1718–1722.
OpenUrl

[94] Karapetis CS,

[95] Khambata-Ford S,

[96] Jonker DJ,

[97] O’Callaghan CJ,

[98] Tu DS,

[99] Tebbutt NC, et al.

[100] 15.↵

Lièvre A,
Bachet JB,
Le Corre D,
Boige V,
Landi B,
Emile JF, et al.
KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res. 1993; 22: 1718–1722.
OpenUrl

[102] Lièvre A,

[103] Bachet JB,

[104] Le Corre D,

[105] Boige V,

[106] Landi B,

[107] Emile JF, et al.

[108] 16.↵

de la Rochefordiere A,
Kamal M,
Floquet A,
Thomas L,
Petrow P,
Petit T, et al.
PIK3CA pathway mutations predictive of poor response following standard radiochemotherapy ± cetuximab in cervical cancer patients. Clin Cancer Res. 1993; 22: 1718–1722.
OpenUrl

[110] de la Rochefordiere A,

[111] Kamal M,

[112] Floquet A,

[113] Thomas L,

[114] Petrow P,

[115] Petit T, et al.

[116] 17.↵

Bossi P,
Resteghini C,
Paielli N,
Licitra L,
Pilotti S,
Perrone F.
Prognostic and predictive value of EGFR in head and neck squamous cell carcinoma. Oncotarget. 1993; 22: 1718–1722.
OpenUrl

[118] Bossi P,

[119] Resteghini C,

[120] Paielli N,

[121] Licitra L,

[122] Pilotti S,

[123] Perrone F.

[124] 18.↵

García-Carracedo D,
Villaronga MÁ,
Álvarez-Teijeiro S,
Hermida-Prado F,
Santamaría I,
Allonca E, et al.
Impact of PI3K/AKT/mTOR pathway activation on the prognosis of patients with head and neck squamous cell carcinomas. Oncotarget. 1993; 22: 1718–1722.
OpenUrl

[126] García-Carracedo D,

[127] Villaronga MÁ,

[128] Álvarez-Teijeiro S,

[129] Hermida-Prado F,

[130] Santamaría I,

[131] Allonca E, et al.

[132] 19.↵

Iglesias-Bartolome R,
Martin D,
Gutkind JS.
Exploiting the head and neck cancer oncogenome: widespread PI3K-mTOR pathway alterations and novel molecular targets. Cancer Discov. 1993; 22: 1718–1722.
OpenUrl

[134] Iglesias-Bartolome R,

[135] Martin D,

[136] Gutkind JS.

[137] 20.↵

Rosell R,
Moran T,
Queralt C,
Porta R,
Cardenal F,
Camps C, et al.
Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med. 1993; 22: 1718–1722.
OpenUrl

[139] Rosell R,

[140] Moran T,

[141] Queralt C,

[142] Porta R,

[143] Cardenal F,

[144] Camps C, et al.

[145] 21.↵

Morgillo F,
Della Corte CM,
Fasano M,
Ciardiello F.
Mechanisms of resistance to EGFR-targeted drugs: lung cancer. ESMO Open. 2016; 1: e000060.

[147] Morgillo F,

[148] Della Corte CM,

[149] Fasano M,

[150] Ciardiello F.

[151] 22.↵

Cizkova M,
Dujaric ME,
Lehmann-Che J,
Scott V,
Tembo O,
Asselain B, et al.
Outcome impact of PIK3CA mutations in HER2-positive breast cancer patients treated with trastuzumab. Br J Cancer. 1993; 22: 1718–1722.
OpenUrl

[153] Cizkova M,

[154] Dujaric ME,

[155] Lehmann-Che J,

[156] Scott V,

[157] Tembo O,

[158] Asselain B, et al.

[159] 23.↵

Deguchi Y,
Okabe H,
Oshima N,
Hisamori S,
Minamiguchi S,
Muto M, et al.
PTEN loss is associated with a poor response to trastuzumab in HER2-overexpressing gastroesophageal adenocarcinoma. Gastric Cancer. 1993; 22: 1718–1722.
OpenUrl

[161] Deguchi Y,

[162] Okabe H,

[163] Oshima N,

[164] Hisamori S,

[165] Minamiguchi S,

[166] Muto M, et al.

[167] 24.↵

Nagata Y,
Lan KH,
Zhou XY,
Tan M,
Esteva FJ,
Sahin AA, et al.
PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell. 1993; 22: 1718–1722.
OpenUrl

[169] Nagata Y,

[170] Lan KH,

[171] Zhou XY,

[172] Tan M,

[173] Esteva FJ,

[174] Sahin AA, et al.

[175] 25.

Berns K,
Horlings HM,
Hennessy BT,
Madiredjo M,
Hijmans EM,
Beelen K, et al.
A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell. 2007; 12: 395–402.
OpenUrl CrossRef PubMed Web of Science

[177] Berns K,

[178] Horlings HM,

[179] Hennessy BT,

[180] Madiredjo M,

[181] Hijmans EM,

[182] Beelen K, et al.

[183] 26.↵

Esteva FJ,
Guo H,
Zhang SY,
Santa-Maria C,
Stone S,
Lanchbury JS, et al.
PTEN, PIK3CA, p-AKT, and p-p70S6K status: association with trastuzumab response and survival in patients with HER2-positive metastatic breast cancer. Am J Pathol. 1993; 22: 1718–1722.
OpenUrl

[185] Esteva FJ,

[186] Guo H,

[187] Zhang SY,

[188] Santa-Maria C,

[189] Stone S,

[190] Lanchbury JS, et al.

[191] 27.↵

Dave B,
Migliaccio I,
Gutierrez MC,
Wu MF,
Chamness GC,
Wong H, et al.
Loss of phosphatase and tensin homolog or phosphoinositol-3 kinase activation and response to trastuzumab or lapatinib in human epidermal growth factor receptor 2-overexpressing locally advanced breast cancers. J Clin Oncol. 1993; 22: 1718–1722.
OpenUrl

[193] Dave B,

[194] Migliaccio I,

[195] Gutierrez MC,

[196] Wu MF,

[197] Chamness GC,

[198] Wong H, et al.

[199] 28.↵

Soria JC,
LoRusso P,
Bahleda R,
Lager J,
Liu L,
Jiang J, et al.
Phase I dose-escalation study of pilaralisib (SAR245408, XL147), a pan-class I PI3K inhibitor, in combination with erlotinib in patients with solid tumors. Oncologist. 1993; 22: 1718–1722.
OpenUrl

[201] Soria JC,

[202] LoRusso P,

[203] Bahleda R,

[204] Lager J,

[205] Liu L,

[206] Jiang J, et al.

[207] 29.↵

Jänne PA,
Cohen RB,
Laird AD,
Macé S,
Engelman JA,
Ruiz-Soto R, et al.
Phase I safety and pharmacokinetic study of the PI3K/mTOR inhibitor SAR245409 (XL765) in combination with erlotinib in patients with advanced solid tumors. J Thorac Oncol. 1993; 22: 1718–1722.
OpenUrl

[209] Jänne PA,

[210] Cohen RB,

[211] Laird AD,

[212] Macé S,

[213] Engelman JA,

[214] Ruiz-Soto R, et al.

[215] 30.↵

Jimeno A,
Shirai K,
Choi M,
Laskin J,
Kochenderfer M,
Spira A, et al.
A randomized, phase II trial of cetuximab with or without PX-866, an irreversible oral phosphatidylinositol 3-kinase inhibitor, in patients with relapsed or metastatic head and neck squamous cell cancer. Ann Oncol. 1993; 22: 1718–1722.
OpenUrl

[217] Jimeno A,

[218] Shirai K,

[219] Choi M,

[220] Laskin J,

[221] Kochenderfer M,

[222] Spira A, et al.

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Biomarkers of cetuximab resistance in patients with head and neck squamous cell carcinoma

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